Plant-animals; a study in symbiosis

PLANT-ANIMALS

STUDY IN SYMBIOSIS

The Cambridge Manuals of Science and
Literature

PLANT-ANIMALS

CAMBRIDGE UNIVERSITY PRESS

HonHon: FETTEK LANE, E.G.

C. F. CLAY, MANAGER

100, PRINCES STREET
TLontoon: H. K. LEWIS, 136, GOWER STREET, W.C.
Berlin: A. ASHER AND CO.
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anti (Calcutta: MACMILLAN AND CO., LTD.

All rights reserved

II!

r^

ill

A. The G-reen Plant-animal (Convoluta roscoffensis).

B. The Yellow-brown Plant-animal ( Convoluta paradocca).

40 times natural size.

PLANT-ANIMALS

A STUDY IN SYMBIOSIS

FREDERICK KEEBLE, Sc.D

PROFESSOR OF BOTANY IN
UNIVERSITY COLLEGE, READING

Cambridge :

at the University Press

1910

PRINTED BY JOHN CLAY, M.A.
AT THE UNIVERSITY PRESS.

AUG 21 1957

With the exception of the coat of arms at
the foot, the design on the title page is a
reproduction of one used by the earliest known
Cambridge printer John Siberch 1521

PREFACE

DURING some ten years' work in a small marine
laboratory in Brittany it has fallen to me
not infrequently to attempt to explain to curious
visitors what were my objects in going to and fro
upon the shore, in wading among the sea-weeds and
in bringing into the laboratory minute, worm-like
animals which represented often my sole "catch."

I discovered that many of the visitors to the
laboratory became interested in the work that
was going on, and that, though they disclaimed a
knowledge of biology, they followed with under-
standing and interest the story of the behaviour
and life histories of "the worms": — indeed, they
succeeded generally in putting to me pertinent and
unanswerable questions with respect to these " plant-
animals."

The pleasant recollection of hours spent in this
way is responsible primarily for my undertaking to

vi PREFACE

contribute this volume to The Cambridge Manuals
of Science and Literature.

If it succeeds in interesting the layman, success
will be due to the severe educational regime to
which my visitors submitted me in their cross-
questionings as to the bearings and objectives of
my biological work.

If it fails, they must bear the blame : for had they
not exhibited a fondness for "Convoluta" I should
scarcely have ventured to publish its doings to the
world at large. Of these friends I would mention
particularly Mr Alfred Dutens, whose interest in
"Convoluta roscofiensis" has been a source of constant
encouragement to me.

The biological facts recorded in this volume are
the outcome of researches carried on for some years
by Professor Gamble and myself, and, subsequently,
without Professor Gamble's co-operation.

Throughout the whole time during which the work
has been in progress, it has benefited more than may
be stated explicitly by the unremitting assistance
rendered by my wife. To her, are due the long and
patient records of the periodic changes of behaviour
of the plant-animals — Convoluta roscoffensis and
C. paradoxa : — records which entailed visits to the
Convoluta colonies at all phases of the tide and at
all hours of the day and night. Though an adequate

PREFACE vii

expression of my thanks to my wife were out of place
here, I beg leave to give myself the pleasure of
acknowledging how great has been her share in
this work.

The original memoirs, giving detailed accounts of
the life histories of the plant-animals, have appeared
in the Quarterly Journal of Microscopic Science. A
list of these memoirs and of other researches to which
reference is made in the text is included in the short
bibliography appended to this volume. The dates,
enclosed within brackets in sundry places in the text,
refer each, to the year of publication of the research
which is cited and indicate that the title of the re-
search in question may be found in the bibliography
under that date.

The black and white illustrations have been pre-
pared specially for this volume by Mrs Seward from
the original drawings made by Miss Dorothea
Richardson in the laboratory at Tregastel. I am
deeply indebted to Mrs Seward and Miss Richardson
for their kind assistance, and to the skill and patience
which they have bestowed on the drawings I offer
a sincere and admiring tribute.

Should the reader find that the main arguments
exposed in the course of the volume are intelligible,
he may, perhaps, be inclined to forgive the use,
which I hope is as occasional as inadvertent, of un-

viii PREFACE

familiar biological terms. I have endeavoured to
avoid this pit-fall, but have doubts as to the com-
pleteness of my success. I shall be obliged therefore
if readers will point out passages which require
elucidation, so that, in the event of another edition
being published, the defects may be remedied.

FREDERICK KEEBLE.

TRE"GASTEL,

COTES-DTJ-NORD,

FRANCE.
September, 1910.

CONTENTS

PART I

THE BEHAVIOUR OF THE PLANT-ANIMALS
CHAP. PAGE

I. Introductory : the worms, Convoluta roscoffensis

and Convoluta paradoxa : their habits and habitats 3

II. The origin and significance of the habits of Con-
voluta roscoffensis and Convoluta paradoxa . 37

PART II

THE NATURE OF THE PLANT-ANIMALS

III. The green cells of Convoluta roscoftensis and the part

they play in the economy of the plant-animal . 75

IV, The origin and nature of the green cells of Convoluta

roscoffensis ........ 100

V. The significance of the relation between coloured

cell- and animal-constituents of the plant-animals 130

BIBLIOGRAPHY 159

INDEX 161

WITH TEXT-FIGURES, 1 — 22.

COLOURED FRONTISPIECE. The Green Plant-Animal, Con-
voluta roscoffensis and the Brown Plant- Animal,
Convoluta paradoxa.

PART I

THE BEHAVIOUR OF THE PLANT-ANIMALS

CHAPTER I

INTRODUCTORY: THE WORMS: CONVOLUTA ROS-
COFFENSIS AND CONVOLUTA PARADOXA: THEIR
HABITS AND HABITATS.

BIOLOGISTS who devote themselves to the investi-
gation of the life histories and life processes of the
lower animals are apt to encounter the criticism:
why expend pain and labour on insignificant creatures
when so much remains to discover with respect to
the higher animals, including man himself?

This perfectly legitimate criticism admits of a con-
clusive reply and, since it is possible that a question
of the kind may arise in the mind of anyone taking
up this book, it shall be answered forthwith. The
reply may take one of three forms. In the first place,
it may be urged that the most important modern
biological discoveries have resulted from researches
into the life histories of the lower organisms. Modern
surgery relies for much of its technique on the results
of investigations into the physiology of the bacteria.
Yet more recently, the experimental elucidation of
the life-histories of the protozoa — the lowest group of

1—2

4 PLANT-ANIMALS [CH.

animals — has laid the foundation of a great and
increasing body of knowledge with respect to the
cause of malaria, sleeping sickness, and other tropical
diseases.

In the second place, it may be urged that, the
more complex the organism, the more difficult it is to
use the results of observations upon it for the purpose
of generalising on important biological problems such
as those of the origin of instinct and habit, or of the
meaning of heredity and the course of evolution.
The higher the organism, the more it has covered up
the tracks along which the species to which it belongs
has travelled. For this reason alone, the study of the
lower organisms is not only to be justified but also
urged on zoologists as one bound to lead to results
of the greatest value.

In the third place, it has yet to be proved that
the higher animals differ in any fundamental respect
from more lowly forms of life. Hence, if, as a
physiologist must hold, such differences as exist
between higher and lower forms are differences of
degree and not of kind, it follows that an increased
knowledge of the nature of the lower organisms
connotes also an increase in knowledge with respect
to the higher organisms.

On these grounds, the patient and exhaustive
study of the lower organisms is to be justified.
Nay more, if the reasons for this study are valid they

i] INTRODUCTORY 5

should serve to induce some of the younger genera-
tion of physiologists to devote their attention to a
field of research both rich in promise and too little
cultivated by the men of science of this country.

Though the results recorded in this volume are
but modest, throwing here and there only a faint
light on the problems which they raise, nevertheless
they suffice to demonstrate that more skilful observers
would, by taking up similar subjects of investigation,
make notable contributions to the science of com-
parative physiology.

Having vindicated the importance of research on
the lower organisms, let us proceed to our task.

The plant-animals whose life histories and habits
form the subject of this volume are two simple,
marine worms, Convoluta roscoffensis and Convoluta
paradoxa (Frontispiece). Both are small, though large
enough to be seen easily by the unaided eye, and both
are conspicuous by reason of their colours. C. ros-
coffensis is dark, spinach green, and C. paradoxa
yellow-brown.

Even among worms they occupy a lowly place.
Unlike the higher members of this group, C. ros-
coffensis and C. paradoxa are unsegmented. Instead
of consisting, like garden worms, of a series of ring-
like pieces, the bodies of our plant-animals are in one
piece and, consequently, bear no ring-like markings

PLANT-ANIMALS

[OH.

s.

S.

II.

Fig. 1. The distribution of the colonies of Convoluta roscoffensis on
the sea-shore. I. at spring-tidal periods (low water) : II. at
neap-tidal periods (low water). Though a colony remains fixed
in position, its size waxes with the spring tides and wanes with
the neap tides. C, C = the colonies3. S. = sea

i] INTRODUCTORY 7

on their surfaces (Frontispiece). Imagine a minute,
elongated fragment of a most delicate leaf, some J in.
long by i^ in. broad, and you have a picture of
C. roscoffensis. Imagine, further, myriads of such
green, filmy fragments lying motionless on moist,
glistening patches of a sunny beach between tide-marks
and you see the species in its native habitat (Fig. 1).
To find C. paradoxa at home it is necessary to follow
the receding tide, to gather handfuls of the brown
seaweeds (Fig. 2) which are exposed towards the low-
water limit of the larger tides and to allow the tips
of the weeds to dip into water in a white dish. Singly
from their hiding-places chubby, brown C. paradoxa
come gliding down with rounded "head" and pointed
"tail" to swim uneasily in the water of the dish.
C. roscofiensis is pre-eminently gregarious, C. paradoxa
by comparison is solitary. Sand from a Convoluta
patch scooped up in a cup contains many thousands
of C. roscoffensis ; a patient fishing throughout the
time of low tide may result in a catch of fifty, or at
most a hundred, specimens of C. paradoxa.

The surface of the bodies of the plant-animals is
somewhat slimy ; particularly in C. roscoffensis, and
is covered by fine cilia (Fig. 3) which, during the life
of the animals, are in constant motion. The cilia,
which are protoplasmic projections from the super-
ficial cells, serve, by their unceasing movements, to
row the animal through the water.

8

PLANT-ANIMALS

[CH.

C. paradoxa possesses, in addition to cilia, occa-
sional, stouter, bristle-like structures which stick out
from its body, chiefly in the "tail" region (Fig. 16,
p. 84). These structures serve, when put in action
by the animal, to pin it down and thus enable it to
stop and stick in any position.

Fig. 2. Convoluta paradoxa (C) attached to sea-weeds
of the paradoxa zone. (Magnified eight times.)

In both animals, the sides of the body are flexed
beneath the under surface, and together form a groove
which, in C. paradoxa, serves to fit the animal saddle-
wise to the fine sea-weeds over which it glides (Fig. 2).
This animal, in its general progress, appears almost
to flow over the substratum on which it is moving.

i] THE STRUCTURE OF CONVOLUTA 9

Occasionally, however, on meeting with an obstacle it
rears its head-end, caterpillar-wise, relaxes the grip
of its flexed sides, readjusts them to the surface and
glides on with stealthy motion.

Though we have called C. roscoffensis and C.
paradoxa simple worms, it is not to be inferred that
the structure of their bodies is really simple. Both
species possess a well-defined nervous system and
efficient sense-organs. At the front or "head" end
of the body, on the upper surface, a little way behind
the anterior end, lie two eyes right and left of the
median line (Frontispiece and Fig. 3). Though of the
simplest construction, each consisting of a minute
spot of orange pigment lying over nervous tissue,
the eyes are efficient for distinguishing light of
different intensities. Numerous orange-pigmented
glands, scattered over the surface of the body, function
probably as accessory eyes. Between the two eyes,
in the median line on the dorsal (upper) side of the
body of either species, lies the otocyst (Frontispiece
and Fig. 3, OT). It consists of a hollow sphere of
nervous tissue enclosing a space within which lies a
small lump of chalk.

Like a pea in a thimble, the heavy, chalky mass,
or otolith, lies freely in the otocyst, and, if the position
of the animal change with respect to the line of
action of gravity, — the vertical — the otolith falls or
rolls on a new part of the otocyst- wall. Pressing on

10 PLANT-ANIMALS [CH.

this area it acts as a stimulus to the nervous tissues
beneath. As the result of stimulation of this tissue,
nervous impulses may be despatched to the muscles
of the body, and, causing them to contract, give rise
to movements of the body which are definite in
direction.

Thus the otocyst serves as an indicator of the
line of gravity ; in other words it acts as the organ

Fig. 3. Young Convoluta paradoxa. C = cilia covering the surface
of the body. OT = otocyst. OC = eyes. V = empty digestive
vacuoles.

for gravi-perception. By its means, the animal is able
to orientate itself with respect to the vertical, and
so to find its way downward or upward.

That the otocyst does indeed serve this end
has been established by experiments with other
animals, and may be inferred in the case of C. ros-

i] THE STRUCTURE OF CONVOLUTA 11

coffensis from the following facts. Occasionally,
among just-hatched larvae specimens occur which
fail to respond like their fellows to gravitational
stimulus. Such specimens are found, on microscopic
examination, to lack properly developed otocysts.
For example, if numbers of C. roscoffensis larvse are
taken up with water into a glass tube and the tube
is shaken slightly, the animals come down, some
tumbling, some curvetting. These animals in general
respond to vibration by a geotactic movement — that
is, one having reference to the line of action of
gravity — but the one or two, devoid of otocysts, fail
to descend, remain glued to the side of the tube and
are dislodged with the greatest difficulty.

As indicated already, the bodies of Convoluta
possess a well-developed system of muscles by the
ordered contractions of which the movements of the
animals are effected.

The digestive system is of a primitive order. A
well-developed mouth, capable of a wide gape, occurs
on the under sl3e of the body rather nearer the
" head " than the " tail " end. The mouth communi-
cates by a short gullet, not with a distinct digestive
tube, but with a loose, central tissue. Hence food
which is ingested passes through the mouth to the
gullet whence it is distributed to improvised spaces
or vacuoles in the tissues (Fig. 3). In these vacuoles
it is digested. The undigested residue is discharged

12

PLANT-ANIMALS

[CH.

at any point of the body, generally, however, toward
the hinder end.

Neither species of Con voluta possesses a circulatory
system. In the absence of heart and blood-vessels, the
distribution of the nutritive substances derived from
the food is effected in a primitive manner, the materials
being passed from cell to cell.

Fig. 4. Convoluta paradoxa. a. Seen from ventral surface, showing
the folds of the sides of the body. b. An animal with nearly
ripe eggs (E).

There is, moreover, no excretory apparatus, and
the waste products are not discharged from the body
but remain and accumulate in the tissues.

Both C. roscoffensis and C. paradoxa are herma-
phrodite, each animal possessing male and female
reproductive organs, the essentials of which are, re-
spectively, spermatozoa and egg-cells. The eggs are
numerous and attain to so considerable a size that

i] THE STRUCTURE OF CONVOLUTA 13

they may be seen lying in rows in the bodies
of "ripe females," that is, animals in the female
stage (Fig. 4, b, E). The eggs are fertilized in the body,
though the spermatozoa which eifect fertilization
are derived from another individual of the same
species. After fertilization, the eggs are discharged
in groups or clutches of from about eight to fifteen
or more. As it is extruded from the body the
egg-clutch becomes surrounded by a transparent,
mucilaginous, sticky capsule secreted by the glands
on the surface of the skin. A clutch of eggs of

Fig. 5. Egg-capsule of Convoluta paradoxa. Each egg is contained
in an egg-membrane and the group of eggs is enclosed by a
common capsule. (Magnified twenty times.)

C. roscoffensis is recognisable to the trained eye as
a minute, more or less transparent sphere of about
the size of a small pin's head. The egg-clutch of
C. paradoxa is of a similar size ; but, owing to the
presence of pigmented granules, it is of a rufous
colour (Fig. 5).

C. roscoffensis lays its eggs on the beach just
beneath the surface of the sand : C. paradoxa deposits
them on the fine sea-weed lower down the shore.

14 PLANT- ANIMALS [OH.

The habitat of C. roscoffensis is restricted and
localised (Fig. 1). This gregarious species occurs
within a well-defined zone of the foreshore of sandy
beaches of Normandy and Brittany. Elsewhere it is
unknown.

An observer, walking at low tide seaward across
a golden beach in Brittany, passes scattered granite
rocks scantily clad with yellow-brown patches of
seaweed adventuring landward and before he reaches
the main belt of brown seaweeds, some yards land-
ward of the thin line of green Cladophora which lies
bleaching in the sun, he may see dark, spinach-green
glistening patches — the colonies of C. roscoffensis.
He must tread softly lest the patches melt away
at his approach. The colonies may extend for
many yards as dark green, irregular strips running
more or less parallel with the shore-line, or they may
consist of apparently disconnected patches varying in
size from an inch or so to a yard or more across. From
the intervals between the colonies, the animals are
not absent. Though they are not to be seen, they
may be smelt. Sand from a part of this roscoffensis
zone where no animals are visible, when squeezed
between the fingers, emits from the crushed, occasional
Convolutas contained in it a pungent and evil smell.
The odour, which is like that of decaying fish, is due
to the volatile trimethyl amine which is produced
by the animal.

i] THE HABITAT OF CONVOLUTA 15

On a peaceful beach, in quiet times, when storms
and tourists are absent, the colonial patches of C.
roscoffensis keep their respective outlines with sur-
prising constancy. Day after day the several patches
may be recognised, waxing in size with the spring tides,
waning with the neap or slack tides (Fig. 1) : larger,
also, on any day soon after the tide has receded
from their borders; smaller, just before the rising
tide invades them. At certain times, the multitude of
individuals which make up a patch may be seen lying
lethargic and motionless, bathed in the sunlight and
the film-like stream of drainage sea- water which oozes
from the sand and flows over them seaward. On days
of bright sunshine, in particular, the animals lie very
still ; on duller days, a constant gliding too and fro of
these minute films of living matter is to be observed
within the confines of a colony. It is on such occasions
that the observer must tread softly, for C. roscoffensis
is so sensitive to vibration that his heavy, approach-
ing tread may send it to earth with lightning speed.
How quickly the animals may make their descent
from the surface may be judged from the illustration
(Fig. 6) which depicts two photographs of a colony,
the second taken at an interval of five minutes after
the first. Three gentle taps on the sand, after the first
photograph was taken, served as the signal for retreat.
At that signal, the army, many millions strong, vanished
with amazing swiftness and took cover underground.
Lest the words "many millions" should seem to

16

PLANT-ANIMALS

[CH.

savour of exaggeration, it may be said that one colony
of moderate size — extending over some two square
yards — was found by estimation to contain 5,600
million individuals. Of such flaky thinness are these
animals that as many as 28,000 may be packed in a

n.

Fig. 6. Kesponse of C. roscoffensis to vibration. Eeproductions of
photographs of a colony. I. before, II. five minutes after the
sand had been tapped lightly with the foot. The dark patches
in I. represent vast numbers of the animals which in II. have
disappeared almost entirely below the surface of the sand.

space measuring one cubic centimetre. A search on
dark nights at low tide in the roscoffensis zone fails to
reveal any of the animals upon the surface. In such
circumstances they remain just beneath the sand.
On moonlight nights, some, but not many, may be

i] THE HABITAT OF CONVOLUTA 17

seen, by the light of a lantern, lying in the river-films
of their diurnal stations.

Except for a rich micro-flora and -fauna of diatoms,
bacteria and infusoria, except for a rare, solitary
enemy — another worm, a species of Plagiostoma, which
shovels live Convolutas by the hundred into its capa-
cious body — except for an occasional, small shore-crab,
picking its way with rolling but deliberate gait over
the patches, C. roscoffensis enjoys undisputed posses-
sion of its tract of foreshore. Though the wastage
from each colony must be prodigious, every incoming
tide taking toll, yet the species, fecund and resource-
ful, rises superior to the circumstances of its environ-
ment and maintains itself in the strange situation
which fate has chosen for it.

The roscoffensis zone (Figs. 1 and 7) is as localised
as the range of distribution of the species is restricted.
The upper limit of the zone is marked by the level
reached by high water at the slackest of the neap tides :
for, further landward, C. roscoffensis could not obtain
at all tidal periods the diurnal plunge-bath without
which it does not thrive. Risk of desiccation bars
its more landward advance. The lower limit of the
zone is but a few yards seaward, for C. roscoffensis
loves the light and ensues it.

At every making tide, this zone is submerged and
C. roscoffensis becomes a submarine plant-animal
sheltering beneath the surface of the sand out of

K. 2

18 PLANT-ANIMALS

reach of the shock of the waves. At every falling
tide, as the receding waters lay bare the zone, C. ros-
coffensis, rises to the surface of the sand and becomes
a land plant-animal, or rather, a sedentary denizen
of the filmy rivers which have their sources in
the sand flooded by water when the tide was full.
Where the springs of drainage-water reach the sur-
face and become rivulets cutting seaward courses, is
the upper limit of the C. roscoflensis zone. Thus the
colonies are so situated on the beach that they are
bathed continuously in running water and receive the
maximum of light-exposure during low water at all
tidal periods. Records kept during a lunar month
show that the time of exposure during low tides is
very fairly constant. The time during which C.
roscoffensis lies on the surface is, on the average, five
and a half hours, and ranges from four and a half to
six hours. Twice during twenty-four hours the ros-
coflensis zone is submerged and the animals live a life
of darkness underground : twice the zone is uncovered
and the animals are free to rise to the surface of the
sand (Fig. 7). By fixing its station and adjusting its
habits, C. roscoflensis succeeds to a remarkable degree
in simplifying its environmental conditions. In that
station, periods of inundation succeed periods of ex-
posure at fairly regular intervals, and, by synchronising
its rhythmic movements up to the surface and down
below the surface with the movements of the tides,

I]

THE HABITAT OF CONVOLUTA

19

C. roscoffensis adjusts its working days to the rhyth-
mic changes of its environment. How remarkable is
the rhythmic movement up and down we shall pre-
sently discover.

Fig. 7. Habitats of C. roscoffensis and C. paradoxa shown in relation
with the rise and fall of the tides during a lunar period.
S = spring tides. N=neap tides. Eosc. zone = habitat of
C. roscoffensis. Parad. zone = habitat of C. paradoxa. The
position of colonies of C. roscoffensis is just below the high-water
level of the slackest tides. The habitat of C. paradoxa is un-
covered at low water except during the slacker neap tides.

Leaving the C. roscoffensis zone and passing the
rank, brown sea-weeds left high and dry by the tides,
the observer paddles into the shallow water, or, if the
tide is a big one, walks almost dry shod and sees the
long, yellow bands of another sea- weed (Ascophyllum)
swaying beneath the water of the pools or lying

2—2

20 PLANT-ANIMALS [CH.

prone on the soft, grey ooze of the sea-floor. The
extremities of the Ascophyllum are clothed with tufts
of fine, epiphytic brown and red sea-weeds. Further
out, as the tide continues to fall, the browner weeds
are becoming uncovered ; first, the dichotomous straps
of Himanthalia which spring from button or saucer-
like stalks attached to the rocks, and then the finger-
like Pycnophycus (Fig. 2) which extends beyond the
seaward limits of even the biggest spring tides. It is
among the fine weeds attached to Pycnophycus that
C. paradoxa is to be found. On dangling these weeds
in water, the animals come out, but as single spies
not in battalions like C. roscoffensis which lies in
swarms thirty yards further up the beach. The
abode of C. paradoxa is less circumscribed than that
of C. roscoffensis and shifts with the tides. At the
onset of the spring tides, minute specimens may be
taken from among the epiphytic weeds attached to
the most landward of the brown sea-weeds (Fucus).
During subsequent spring tides, the animals must be
sought lower down the beach in the zone occupied
by Himanthalia and Ascophyllum ; whilst, yet later
in the same series of springs, C. paradoxa is to be
found only in the Pycnophycus zone. Just where
that dark brown weed ceases to be exposed at low
water of the largest spring tides is the further limit
of the paradoxa zone (Fig. 7). Like the Greek sailors
described in Eothen C. paradoxa hugs the shore. Ex-

i] THE HABITAT OF CONVOLUTA 21

posed now to the violence of the sea and now to the
hot sun striking on the drying, emerged rocks and
weeds, C. paradoxa has chosen its abiding place. But,
unlike C. roscoffensis, C. paradoxa fails to finds in its
station a regular recurrence of change, and hence it
is constrained to shift its station during the lunar
periods. At times of slack tide, the seaward part of
the C. paradoxa zone is submerged continuously and
the light which reaches the animals clinging to weed
some feet below the surface is too feeble for their
requirements. Hence, during such tides, C. paradoxa
edges up landwards to the shallower water and reaches
so far as the Fucus zone. During the spring tides, this
latter zone is left high and dry for hours and hapless
C. paradoxa stranded there would suffer from the
intense isolation and also run the risk of desiccation.
So, as the tides increase, it works its way down the
beach, reaching, at the median spring tides, to the
more seaward weeds, and at the largest springs, when
these weeds may no longer harbour it in submerged
peace, it treks again yet further toward the sea and
takes up its station among the tangle of fine weeds
which hang in tassels from the finger-like, dark brown
Pycnophycus. During the slack periods, at low water,
when the landward part of the Pycnophycus zone is
uncovered, C. paradoxa creeps into the deepest re-
cesses of the matted, emerged weeds. Soon, the
making tide covers the Pycnophycus with an in-

22 PLANT-ANIMALS [CH.

creasing load of water and C. paradoxa, clinging
painfully to the floating, swaying weed, finds itself
exposed to a light intensity none too high for its
requirements.

Unlike C. paradoxa which, as we see, migrates
periodically, its Sittings coinciding with the phases
of the moon, C. roscoflensis, having selected its station
on the beach, maintains it in spite of time and tide.
Small wonder therefore that the latter organism
has learned to respond so swiftly to vibrations
that it sinks below the sand at the approach of
heavy feet. How sure and swift are the uprisings
and downlyings of C. roscoflensis may be learned by
standing at the water's edge near by the situations
known to be occupied by C. roscoflensis colonies.
Scarcely has the tide run oif them when a faint green
discolouration of the sand marks the contours of each
colony, and before the water has receded more than
a few yards the dark greenness of the patch indicates
that all the animals have risen to the surface. Or if,
when the sea is smooth, we watch the incoming tide
making its way with gentlest approach toward the
patches, we see the animals inert and lying massed
together, bound into scum-like lumps by the muci-
laginous excretion of their bodies. They lie motion-
less, oblivious of the lapping waves a yard or so away.
Then, as the latest wave washes over the patch,
lethargy gives place to action and, in an instant,

i] THE HABITAT OF CONVOLUTA 23

C. roscoffensis is gone. On stormy days, when the
making tide announces its landward progress angrily
—thundering like ramping clouds of warrior horse —
the reverberations of the sand send signals to the
colonies which make their dispositions underground
long before the breaking waves can reach or damage
them. All these ordered goings and comings may
the observer see on any day on any beach in Brittany.
But, to discover more precisely the physiological
methods of these purposeful movements, the labora-
tory must take the place of the beach, and simple
scientific methods must supplement bare observation.
In this way, it is possible to refer movements, so pur-
poseful as to suggest volition, to simple, non-conscious,
nervous responses to one or more of several stimuli,
the chief of which are gravity and light.

Before, however, we investigate the living animals
in the laboratory we may note yet another example
of rhythmic behaviour in our plant-animals.

However carefully the observer seeks at low water
among the exposed weeds of the paradoxa zone, he will
find no animals bearing ripe eggs. As the tides be-
come large enough to permit of approach on foot to
that zone, the animals which he obtains are, for the most
part, minute, immature specimens. On succeeding days,
the catch consists of larger animals, till, during the
latest spring tides, it is composed chiefly of adults, many
of which may contain unripe eggs. Then comes a period

24 PLANT-ANIMALS [CH.

of slack tides when the paradoxa zone is constantly
submerged beneath ten feet or more of water. At
the succeeding spring tides, the same sequence of
immature, young and adult animals is obtained by
the collector. The absence of mature females and
of deposited egg-capsules is not to be explained by
a migration of gravid females to some other place
more convenient for the purpose of egg-laying ; for,
now and again, a solitary capsule may be found during
the latest spring tides glued to the weed of the
paradoxa zone. By hatching experiments carried
out in the laboratory, it may be demonstrated that
the time of maturing of the animals coincides with
a definite tidal period. It takes either a month
or a fortnight for the animals to become mature.
They reach maturity at neap-tidal periods. At the
beginning of these periods, or soon after, when the
zone is submerged continuously for some seven or
eight days, C. paradoxa lays its eggs. No matter
how the conditions are altered in artificial hatching
experiments, C. paradoxa is faithful to its habit: as
indicated by the diagram (Fig. 8), which records the
results of such experiments, the females lay their
eggs only during the neap tides.

Nor is it without significance that the large
yellow-brown eggs of C. paradoxa, rich in food-
yolk, hatch with extraordinary rapidity. Within
twenty-four to forty-eight hours of the time of lay-

I]

PERIODICITY IN CONVOLUTA

25

ing, the larvae, after circling actively within the
capsule, burst the walls thereof and escape. Thus
they have, during the remainder of the neap-tidal
period, some days of comparative tranquillity and
uniformity of conditions. Not for some days yet will
they be exposed to the full to the chances and changes
which must beset their adult lives. They are born
as submarine animals, and in their earliest days are
spared to some extent the buffetings which shall
be theirs when, with the advent of the spring tides,
they are, now, clinging to fragile weed dashed against

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Fig. 8. Periodicity of egg-laying and hatching of C. paradoxa. The
shaded band shows the position of the Paradoxa zone with
respect to low water-marks of spring and neap tides. The
undulating line, joining up the low water-marks of successive
day-tides, is obtained by marking off," along the verticals indi-
cating successive days, from a zero line above, the amount of
vertical descent (in decimeters) of each day's tide. On those
days when the undulating line falls below the shaded band, the
Paradoxa zone is uncovered during low water ; on those days
when the low water-line lies above the shaded baud, the zone is
continuously submerged. The dots represent egg-capsules, the
crosses signify larvae hatched ; the positions of dots and crosses
give the dates on which the capsules were laid and larvaB
emerged.

26 PLANT-ANIMALS [CH.

the rocks and, now, still clinging to the weed, left
stranded, prone upon the ooze beneath the glare of
an August sun.

With C. roscoifensis, also, egg-laying is a periodic
phenomenon, though, in this species, the times at
which it occurs coincide not with the beginnings of
neap tides but with the onset of the springs. A
colony of C. roscoifensis is indeed a well-drilled army.
Not only do all its members take cover as one unit at
a given signal, not only do the individuals keep their
ranks when the order comes to climb to the surface
once again, but they are born together, grow up to-
gether, mature at the same time and lay their eggs
simultaneously. As a consequence, it is easy to obtain
large numbers of egg-capsules, though only at definite
tidal periods. To secure them, all that is necessary
is to visit a fertile colony at low water during one of
the earlier spring tides, tap with the foot and thus
drive C. roscoffensis below the surface, scoop up a
little sand, shake it with sea-water in a glass tube,
and isolate the slow-sinking, transparent capsules.
It is still easier, however, to rear them in the labora-
tory. By collecting a cupful of sand and C. roscoifen-
sis just before the onset of a series of spring tides,
bringing the cup into the laboratory, adding a little
sea-water, leaving it till the plant-animals have col-
lected on the surface, scooping them oif with a
watch-glass and putting them with sea-water in a

i] PERIODICITY IN CONVOLUTA 27

large glass vessel, hundreds of egg-capsules may be
obtained within a few days. The laying continues
for a week or more and then, when the time of the
slack tides arrives, it ceases, even though some of
the animals are yet carrying mature eggs. After a
barren fortnight, egg-laying begins again. Both the
animals which failed to bear and those which pro-
duced eggs contribute to the fortnightly crop. The
mode of egg-laying of C. roscoffensis is in some
respects peculiar. Occasionally, the eggs are dis-
charged separately one or two at a time ; but more
often they are contained, as has been stated, in a
common, gelatinous capsule. It happens frequently
that oviposition results in a rupture of the tissues
of the parent. The body becomes torn and may even
break across the middle. The anterior end crawls
away and, behaving like an intact animal, heals its
wounds, regenerates its lost parts and recovers
completely. The tail end remains near the egg-
capsule, and exhibits ceaseless, revolving, " circus "
movements, swimming in devious spirals ; then it
comes to rest and finally disintegrates. Unlike
C. paradoxa, C. roscoffensis is slow in hatching.
After about four days, the larvse begin to revolve
actively within the capsule-membrane, then at the
fifth to the seventh day after the eggs were laid, the
egg-membranes split equatorially and the society of
larvae is set free to creep and swim within the common

28 PLANT-ANIMALS [CH.

capsule. Suddenly they leave it, passing with ease
through the mucilaginous wall, though they not
infrequently return now and again to the capsule
after enjoying a short spell of activity — a fact the
significance of which we shall have occasion to
comment upon later.

In seeking an explanation of the significance of
the fortnightly periodicity in egg-laying, it is easy to
conclude that the periods chosen by C. roscoffensis
are the most convenient for this purpose. For in
summer, to which period of the year these observa-
tions apply, low water of spring tides occurs about
midday and midnight. Now, as we have learned, when
the roscoffensis zone is uncovered during the darkness
of night the animals do not remain on the surface.
Hence, during the spring tides, C. roscoffensis has an
uninterrupted period of some eighteen hours in which
to lay its eggs. At other tidal periods, its leisure
would be less, for, as the tide runs off the patch, the
animal must come up to the light and it must re-
main up till the returning tide gives the signal that its
vigil is at an end. In short, whereas, during the
neap-tides, at which periods low water occurs in
early morning and late afternoon, C. roscoffensis has
two up- and two down-periods, during the springs it
has only one period of compulsory " upness " in each
twenty-four hours.

The weak point, however, of all such teleological

i] PERIODICITY IN CONVOLUTA 29

explanations is that they tend to exercise the in-
genuity of men of science rather than to advance
our knowledge of physiology. To which it may be
answered that adaptation is as much a property of
protoplasm as weight is a property of matter, and
that the biologist is performing a service in showing
how deep-bitten into the organism are the adaptations
whereby it adjusts itself to its environment.

To this the critic replies : This is very true, but to
rest content with a teleological explanation, to say
that this animal does such and such a thing because
it is convenient or useful for it to do that thing
is to renounce profound investigation. Before this
can be regarded as the proper philosophical attitude
toward life, the resources of chemistry and physics
must be exhausted, and the behaviour under con-
sideration must at least be proved not to be due to
a chemical or physical change induced by some factor
or factors of the environment.

In other words, the least the physiologist can do
is to attempt to discover how the adaptive trick is
performed by the animal which exhibits it.

An admirable example of an apparently adaptive
character, which is capable of a simple physical
explanation, is given by Loeb (1909) in his brilliant
essay on the influence of environment on animals.

The two species of Salamander, Salamandra atra
and S. maculosa occupy distinct stations. The former

30 PLANT-ANIMALS [CH.

species occurs in dry alpine regions of relatively low
temperature ; the latter, in lower regions with plenty
of water and of higher temperature.

In the dry, alpine regions S. atra deposits eggs
which hatch out as land-animals ; in the wet lowlands,
the eggs laid by S. maculosa contain embryos in a
less advanced stage of development. The young,
when born, are gill-bearing and complete their de-
velopment whilst leading an aquatic mode of life.
Thus each species is adapted to the physical con-
ditions of its environment.

But it has been shown that if S. atra is exposed
to lowland conditions, that is, to a moist atmosphere
and a relatively high temperature, it lays its eggs
earlier, the young hatch out in the gill-bearing stage
and development is completed during their life
as independent, aquatic animals. Conversely, if
S. maculosa is exposed to alpine conditions, oviposition
does not take place till the embryos have passed
beyond the aquatic, gill-bearing phase. Therefore,
in these circumstances, they are born as land-
animals.

Hence the adjustment of each species to its
environment is due to the direct effect of certain of
the physical conditions of that environment on the
course of development of the embryos. The fact of
adaptation is not denied, but the mechanism whereby
it is effected is discovered, and the way made clear

i] PERIODICITY IN CONVOLUTA 31

for a fuller physiological analysis of the mode of
reaction of protoplasm to physical stimuli.

The problem with respect to periodicity of egg-
laying by Convoluta requires us to ascertain whether
it is possible to refer the periodicity to any definite,
recurrent physical condition of its natural environ-
ment.

The facts about to be related appear to indicate
that this is possible.

It may be premised that if adult C. roscoffensis
are kept in darkness for some time previous to the
full development of their eggs, no egg-capsules are
laid. The lack of egg-production on the part of
dark-kept animals is due to the fact that animals
kept under such conditions become starved and, as
a consequence, incapable of supplying the eggs with
food-materials. But if a similar experiment is made
with animals containing eggs in an advanced stage of
development and already supplied with plenty of
food-materials, it is found that the number of egg-
capsules produced by animals kept in darkness is
actually greater than that produced by animals which
are exposed throughout the day to the light. Hence
we may infer that exposure to long spells of twelve
or more hours of light is unfavourable to the maturing
or deposition of eggs. Further experiments on similar
lines show that egg-laying reaches its maximum when
the animals are subjected daily to one short spell of

32 PLANT-ANIMALS [CH.

six hours' light-exposure followed by a long spell of
eighteen hours' dark-exposure. But — and the fact is
remarkable — these conditions of light and darkness
are precisely those to which C. roscoffensis is exposed
during the spring tidal periods at which its eggs are
laid habitually. At such periods, low water of suc-
cessive tides occurs about the middle of the day and
of the night, and hence, in twenty-four hours, the
C. roscoffensis zone is uncovered once during day-
time and once during night-time. So it comes about
that, during the spring tides, C. roscoffensis is exposed
for about six hours to the light and for the rest of
the twenty-four hours is in darkness. Therefore, as
the laboratory experiments show, of all the daily
changing light conditions to which it is subjected
throughout a lunar period, those which obtain at
spring tide are most favourable to the deposition of
egg-capsules.

In ascribing to light a leading rdle in determining
the periodicity of egg-laying we have the support of
not a few well-established biological facts. Thus the
profound influence which light exerts on plants, both
on their development in general and on their flower-
production in particular has long been recognised.
Perhaps the best-known example of this influence
is afforded by the common ivy. It is a fact of
general observation that ivy growing on a wall
rarely if ever flowers, though when climbing over

i] PERIODICITY IN CONVOLUTA 33

an arch exposed on all sides to the light it blooms
freely. These effects of illumination on flower-
formation have been investigated by Vbchting, whose
researches are summarised by Goebel (1900). In
order that plants may form flowers in a normal
way, the illumination must not sink below a certain
amount which is very unequal in different species.
If illumination is allowed to sink below the required
amount, the size of the whole flower or of its individual
parts is diminished and, with decreasing illumination,
a stage is reached at which the formation of flowers
ceases.

Similar phenomena are doubtless common among
animals though they have not been investigated
systematically. Thus, though the phenomenon is
not one of reproduction in the strict sense, we may
cite Loeb's account (loc. cit.) of the effect of light in
inducing regeneration of the polyps of the Hydroid
Eudendrium racemosum. If a stem of this Hydroid,
covered with polyps, is put into an aquarium, the
polyps fall off very soon. If the aquarium is in
darkness, no regeneration of the polyps takes place
even after several weeks ; but, when they are exposed
to the light, new polyps form in the course of several
days. We may suppose that light favours the forma-
tion of definite substances which are the pre-requisites
for polyp formation.

Similarly, Ave are bound to conclude from our
K. 3

34 PLANT-AXIMALS [CH.

experiments on C. roscoffensis that a spell of illumi-
nation of brief duration favours one or other of
the series of processes which results in egg-laying,
that a longer or shorter spell of illumination is un-
favourable to this process, and that, when animals are
subjected to these unfavourable conditions, many of
them, though they are carrying eggs in an advanced
stage of development, remain sterile.

With respect to the periodicity of egg-laying by
C. paradoxa it is not so easy to refer the periodic
character of this event to the influence of light. It
is noteworthy that other littoral, marine organisms,
(certain brown algae) living in almost identical habitats,
exhibit an identical periodicity with respect to their
reproductive processes.

This, according to Williams (1898), is the case
with the brown sea-weed Dictyota dichotoma, and
subsequent observers have shown it to be true of
other marine algse. Not only does Dictyota liberate
successive crops of fertile eggs at fortnightly periods
but it sheds them at the same point in the tidal
period as that chosen by C. paradoxa for the dis-
charge of its egg-capsules. In either case, the eggs
are liberated some three to five tides after the
greatest springs. During the subsequent tides of
smaller amplitude, the zone which forms the habitat
of both sea-weed and plant-animal is continously sub-
merged. Hence we can scarcely escape the conclusion

i] PERIODICITY IN CONVOLUTA 35

that the period selected for egg-laying has reference
to the greater security which is offered during the
first days of larval life. Born into the world at this
period, the animals and the plantlets have some days
of submerged grace before they become subjected
twice daily to such extreme environmental changes as
occur at other phases of the tidal sequence.

Thus, driven back provisionally on a teleological
explanation, we may interpret the significance and
origin of periodicity of egg-laying in the following
way. One condition for survival of the species
C. paradoxa and of Dictyota is that the just-liberated
young shall be for some days after birth continually
submerged : that, for one reason or another ultimately
connected with nutrition, the maturing of these
marine organisms and the development of their
sexual cells requires a period of fourteen days, and
that the organisms fit their fortnightly periods into
the tidal periods in such a way that they reach their
climaxes at the most convenient moments. As the
waving flag of the guard gives the signal for the
train to start, so change of light intensity appears
to give the signal for the maturing of the sexual
organs and thus secures their liberation at the proper
moment.

Whether such bi-lunar periods of fertility ex-
hibited by littoral, marine organisms have any bearing

3—2

36 PLANT-ANIMALS [CH. I

on similar periodic phenomena exhibited by the
higher land-animals it is impossible to say ; though
it is tempting to think with "The Lady from the
Sea," "that we all are descended from sea-animals,
and that if we had only accustomed ourselves to live
our lives in the sea we should by this time have been
far more perfect than we are."

CHAPTEE II

THE ORIGIN AND SIGNIFICANCE OF THE HABITS OF
CONVOLUTA ROSCOFFENSIS AND CONVOLUTA
PARADOXA.

THE fact which stands out most prominently from
open-air observations of C. roscoffensis and C. para-
doxa is that the behaviour of these animals is
complex and purposeful. By some means or other
they create for themselves an ordered life, in spite of
the welter of change in their environment. Through
the ever-varying conditions of the world in which
they live, they thread their consistent way as surely
as we, with conscious self-control and agility, pick our
ways safely through the crowded traffic of the street.

We have now to endeavour to ascertain the
nervous components of the complex behaviour of
our plant-animals; to learn, by the method of ex-
perimental analysis, whether it is possible to refer the
ordered complexity of this behaviour to some few,
simple, nervous acts.

It is a matter of common knowledge that many
organisms, both plants and animals, orientate them-

38 PLANT-ANIMALS [CH.

selves with reference to the directions in which light
and gravity act upon them. A geranium in a cottage
window so disposes its leaves that they receive the
maximum of such light as may reach them. Each
leaf places itself at right angles to the direction of
the incident light. The stem of the plant behaves
differently, bending till its tip is parallel with
the rays, it grows toward the source of light. Light
is the agent, or stimulus, which induces these orien-
tations. The mode of orientation is determined by
the plant itself and has, in each case, a purposeful
significance. The leaves in the window are none too
well illuminated ; the work which they have to per-
form depends on ample light and thus, by their
orientations, they secure for themselves the most
favoured light-treatment.

The root of a plant grows vertically downward
through the soil. When, from one cause or another,
the tip is displaced from the vertical line, the rate of
elongation of the growing region of the root becomes
faster on the upper than on the lower side. A growth-
curvature results, and the tip is carried by the bending
root once more into the vertical line. Here gravity is
the stimulus, and the result of the stimulus is a motor
response — a purposeful growth-curvature. Cut away
the root-tip, and the root, although it be displaced from
the vertical, grows indifferently in any direction till a
new root-tip is regenerated. From such and similar

ii] HABITS OF COXVOLUTA 39

observations Charles and Francis Darwin (1880)
concluded that the power of gravi-perception is
localised in the root-tip. Nor has subsequent criticism
succeeded in invalidating this conclusion.

Now, since the growth-curvature, which results
from the perception by the root-tip of the stimulus
of gravity, occurs in a region of the root — the elon-
gating region — which is separated from the tip by
a region which is not increasing in length, it follows
that perception by the root-tip results in an excitation
of the living substance of its tissues, and that this
excitation gives rise to some change in the tissues
which intervene between the perceptive and motor
regions. This change, of unknown nature, we may
call a nervous impulse, and we may say that, as the
result of excitation consequent to perception, a
nervous impulse is transmitted from the root-tip to
the motor region. Of the nature of this impulse we
know nothing ; nor, for the matter of that, is any-
thing definite known of the nature of any nervous
impulse ; for example, that which travels along a
nerve to a muscle in one of the higher animals. The
" nervous impulse " may well be of chemical nature,
and transmission of such an impulse through living
tissues does not connote definite specialised nerves.
It is as much the property of protoplasm to transmit
nervous impulses as it is of fire to burn, or of a lit
fuse to explode a charge of gunpowder. Protoplasm

40 PLANT-ANIMALS [CH.

is an apparatus for that purpose : as well, of course,
as for other purposes.

Arrived at the motor region, the nervous impulse
sets up an excitation in the protoplasm of that region.
As the result of this excitation, there arises a definite
modification in the hitherto uniform rate of elonga-
tion of the cells of the motor region. The cells of
one side grow faster than those of the other, and a
growth-curvature results by which the tip is carried
back to the vertical position. Such a mode of
nervous action is called a reflex. In every case,
in the simplest, unicellular organism and in the
highest animals, reflex action involves perception,
excitation, transmission to the motor region, excita-
tion of, and motor (or other) response by, that region.
All protoplasm, as we know it, contains the apparatus
required for this series of events, and evolution, as
we know it, has but resulted in the perfecting and com-
plicating of these reflex arcs. We may take the reflex
as the base or primal manifestation of all nervous
activity. In the reflexes of root and stem and leaf,
the stimuli — light, gravity, etc. — which induced them
give rise to the assumption by the root or stem
or leaf of a definite position with respect to the
direction whence the stimulus proceeds. Such
stimuli are therefore called directive stimuli. When
a fixed plant or animal responds to a directive
stimulus by a definite, purposeful curvature we de-

ii] HABITS OF CONVOLUTA 41

scribe the response as tropistic. If the plant or
animal is not fixed but free, it responds by moving
in a definite direction and the response is described
as tactic. Inasmuch as the end of either reaction
is the achievement of a definite orientation and inas-
much also as the fixed plant, not only curves till it
assumes a definite position, but also, having done so,
moves by growth in the direction to which its curva-
ture has brought it, we may use the term tropistic to
describe the reactions of both fixed and free organisms
to directive stimuli.

We have now to consider the tropisms of our
plant-animals.

Brought into the laboratory and placed in sea-
water in a glass vessel near the window, C. ros-
coffensis behaves precisely like the leaf of the
geranium in the cottage window. Each animal turns
to the light, moves toward it and finally exposes
the surface of its body athwart the line of light.
Within a minute or two the reaction is completed.
Swiftly and, as it would seem, inevitably the animals
assemble on the side of the vessel toward the
light, and form a green scum on the surface of
the water. If the vessel is turned round, the
animals release their holds and, either falling like
a precipitate to the bottom or edging round the
side of the vessel, arrive once again at the water's
edge on the side of the vessel directed toward the

42 PLANT-ANIMALS [OH.

light. This mode of response we speak of as a
positively (+) phototropic response.

C. paradoxa, which lives in a shadier situation,
responds to the light of the laboratory by an opposite
movement — a negatively (— ) phototropic response
(Fig. 9, a).

Fig. 9. Phototropism of C. paradoxa : the influence of light-intensity
on phototropic response, a. Mode of response when the light-
intensity is high. b. Mode of response when the light-intensity
is low. The glass troughs containing the animals are represented
(in plan) by oblongs. The troughs standing on a black ground
are represented by the shaded, those on a white ground by the
clear oblongs. The animals are indicated by dots, and the arrows
show the direction of the light.

It is easy to prove, however, that neither the
positive phototropism of C. roscoifensis, nor the oppo-
site mode of reaction of C. paradoxa, is, in reality, an
inevitable reaction. Expose C. roscoffensis suddenly
to a bright light and it recoils (see Fig. 12) — as we
ourselves in similar circumstances may recoil. Place
it in a dim light and it exhibits no phototropistic re-

ii] HABITS OF CONVOLUTA 43

sponse : it has become non-phototropic. On the other
hand, in the gloom of an ill-lit cellar, in which the
light-intensity approximates to that of its habitat
among the masses of brown sea-weed, C. paradoxa
becomes somewhat -f- phototropic (Fig. 9, b).

It is urged not infrequently that reflexes are the
nervous units, unalterable in form, of which behaviour
and higher phases of nervous activity are composed.
The briefest study of the lower animals demonstrates
that, though reflexes may be regarded as units by
the physiological summation of which behaviour
and habit are composed, they may not be regarded
as unalterable and inevitable. No more than con-
scious acts are reflexes the masters of the organism
which exhibits them. They are but servants, and
tropistic reflexes serve the master-organism, to
draw it this way or that according as it is well
that, this or that route be taken. Under un-
changing conditions, both with respect to environ-
ment and with respect to the state of the organism,
the reflex is inevitable. But under such conditions
a conscious act is likewise inevitable. Since un-
changing internal and external conditions are all
but unknown in nature, there will always be scope
for modification in the reflex as in the conscious act.
If the physiologist is called in to act as umpire in
the dialectical game between the advocates of free-
will and determinism, he pronounces the game a

44 PLANT-ANIMALS [CH.

draw. Under abnormal and well-nigh impossible
conditions, the organism, high or low, is an automa-
ton^— the creature of inevitable nervous responses —
reflex or conscious. Under normal conditions of life,
it responds now this way and now that to external
or internal stimuli and so appears to act as a free
agent.

The apparent inevitability of reflexes is but an
indication of habit. When the environmental cir-
cumstances to which an organism is exposed are
comparatively simple or when the organism itself is
not highly differentiated, one or two external agents
may serve it as guides. The organism takes the habit,
for example, of relying implicitly on the stimuli of light
and gravity. By responding to these stimuli, it finds
its proper place with such certainty that other modes
of response to other stimuli are ignored habitually.
Hence, by playing on its habitual tropisms, it is
easy in the laboratory to lure an organism to its
doom.

This we may illustrate by exposing C. roscoffensis
to simultaneous stimulation by light and heat. It
must be premised that the animal, though, for a
marine organism very tolerant of high temperatures,
is negatively thermotropic at about 35° C. At this
temperature it moves in the direction of the colder
water. In order to investigate the behaviour of the
animal with respect to simultaneously applied light-

n] HABITS OF CONVOLUTA 45

and-heat stimuli, large numbers of C. roscoffensis are
placed in sea-water contained in a long glass trough,
the axis of which is parallel with the direction of the
light. Promptly, the animals mass themselves at the
end of the vessel directed to the light. The water
at that end is heated gradually ; but in spite of the
rising temperature, and in spite of its powers of
negative thermotropism, Convoluta remains faith-
fully at its light station, and dies in thousands at its
post. Habitual obedience to the command of light
renders it oblivious of the warning of increasing
temperature, which warning suffices to bring about
the withdrawal of less pre -occupied animals from
dangerous regions. We see in the behaviour of the
plant-animals thus subjected to simultaneous stimu-
lation not an illustration of the inevitableness of a
reflex, but an example of the limitations attaching
to all nervous actions, both reflex and conscious.

The behaviour of C. roscoffensis with reference
to black and white backgrounds supplies a striking
illustration of the fact that circumstances alter re-
flexes. These "background" responses we will now
consider. The choice of a definite background is a
phenomenon exhibited by many sea-shore and aquatic
animals. When offered the alternative of a white or
black background, some animals take up a position
on the one, some on the other. Thus among the
marine Crustacea, certain prawns and also species of

46

PLANT-ANIMALS

[CH.

B

Fig. 10. Diagram illustrating the influence of background (white
or black) on the movements of Convoluta roscoffensis. The
animals are placed in shallow porcelain troughs, the bottoms of
which are half white and half black (shaded). Each dash
represents a Convoluta. A. In uniform light. At. At beginning
of experiment, Convoluta fairly uniformly distributed. A2. After
forty minutes, Convoluta all on white ground. B. In lateral
light (arrows show direction of light). Fifty Convolutas placed
in the white half of li, and fifty in the black half of 2X . 12 and 22
show the results after two minutes : — in 12 ratio on black and
white = f £ ; in 22 ratio = -fo . See text.

n]

HABITS OF CONVOLUTA

47

Mysis station themselves on the black part of a dish
the bottom of which is half black, half white. The
chameleon shrimp, Hippolyte varians, on the con-
trary, selects the white ground (Fig. 10). A similar
behaviour is exhibited by various fishes, trout among
others.

1 I

Fig. 11. Phototropism of C. paradoxa : the influence of background
on phototropic response. The flat, porcelain troughs containing
the animals are represented (in plan) by the oblongs. The bottom
of each trough is half white and half black. In the diagram, the
white ground is indicated by the unshaded, the black ground by
the shaded part of the oblong. The animals are represented by
dots, and arrows show the direction of the light. a. In bright
light, b. In weak light. c. "Choice" of black ground in
preference to white ground.

So striking is the behaviour with respect to
background both of C. roscoffensis and C. paradoxa,

48 PLANT-ANIMALS [OH.

that when specimens of the two animals are put
together into a dish, the bottom of which is half
black and half white, they segregate rapidly and
completely ; C. roscoffensis takes up positions on the
white ground, C. paradoxa on the black ground
(cf. Figs. 10 and 11). The distribution is in accord
with reasonable expectation based on knowledge of
the natural habitats of the two species. C. ros-
coffensis, attuned to a high light intensity, with its
place in the sun, is evidently a bright background
animal ; C. paradoxa, lurking in the shadows of the
weeds, though it also needs light for its growth and
development, is unused to well-lit situations and
seeks in preference the darker background.

But though the selection of ground seems bio-
logically reasonable the question remains, how is it
done ? The hypothesis may be hazarded that it is
a phenomenon of association. C. roscoffensis is, as
we know, positively phototropic. In effecting a
phototropic response, it is bound in ordinary cir-
cumstances to pass from a darker to a lighter
background. The performance of the phototropic
movement is associated with the darker ground, the
achievement or consummation — that .is, a state of
immobility — is associated with the brighter back-
ground. If therefore we adopt the hypothesis,
proposed by Semon, (1904) that environmental con-
ditions, which are contemporaneous with a particular

ii] HABITS OF CONVOLUTA 49

stimulus, are recorded in the "mneme" or unconscious
memory of an organism as integral parts of the
nervous operation initiated by the stimulus and con-
summated by the reaction which it calls forth ; then
it may well follow, as it follows in organisms endowed
with conscious memory, that these environmental
conditions acting alone and in the absence of the
stimulus, may suffice to set in action the nervous
apparatus in the same manner as the stimulus itself
originally set that apparatus in action. Hence the
attendant environmental conditions may produce the
reaction originally called forth by the stimulus.

An example borrowed from Sernon's work (loc. cit.)
may make the idea clearer. A boy throws a stone
at a puppy. The dog is hit and hurt, whimpers and
runs away. The next time the puppy — grown older
and wiser — sees a boy stoop, as though to pick
up a stone, it whimpers and runs away. Linked in
the memory are the hurt, the stone, and the stooping
boy. The hurt supplied the stimulus for whimpering
and flight ; but memory, the constable of the body,
charges the stooping boy with being an accessory to
the act. Henceforth it will advise the avoidance of
stooping boys. Experience consists in the discovery
of short cuts to safety.

So, assuming with Samuel Butler and Hering,
an unconscious memory, or mneme, Semon suggests
that the lower organisms may react to the attendant

K. 4

50 PLANT-ANIMALS [CH.

or accessary stimulus in the absence of the prin-
cipal.

Applying this hypothesis to background reaction,
we assume that dark background, from constant
association with unilateral light, has come to suffice
to stir up the mneme and so to set going the nervous
apparatus which induces a precise muscular move-
ment. Thus, C. roscoffensis, placed on a dark back-
ground, begins to crawl about and continues to do
so. That this interpretation of the origin of back-
ground reaction, contains something of the truth
seems probable from the fact that the movements
performed by the animals on a dark background are,
compared with the business-like, phototropic move-
ments, aimless as to direction. They are non-directive,
chance movements ; but since they continue so long
as the dark background is there to call them forth,
they conduct the animals sooner or later to the Avhite
ground of the particoloured vessel. Arrived there,
the stimulus ceases from troubling and C. roscoffensis
is at rest.

We conclude, therefore, that background, from
being a mere attendant circumstance, an environ-
mental accessory to unilateral light, has come itself
to serve as a stimulus to movements which, by the
devious paths of chance, direct the animals to the
lighter ground.

In nature, under all ordinary conditions, back-

ii] HABITS OF CONYOLUTA 51

ground co-operates with unilateral light to bring
C. roscoffensis to its proper light station — its place
in the sun. Nevertheless background stimulus may,
under artificial conditions, act antagonistically to
that of lateral light and even dominate it.

Thus if two half-black, half-white porcelain
troughs containing a little sea-water are so placed
that, in one, the white half, in the other, the black
half is directed towards the source of light, then, if
some fifty C. roscoffensis are placed in each of the
troughs, whereas in a very short time all the animals
are congregated on the white ground of the first
trough, only about forty per cent, manage to arrive
at and maintain themselves upon the black half of
the second trough (Fig. 10, B).

When positive photo tropism involves the passage
from black to white the movement is executed with
certainty and despatch ; but when it demands a
passage from white to black — a movement against
the grain of habit — there are hesitation, uncertainty,
and many failures. Under yet other conditions, —
when, for example, the intensity of the unilateral
light is lowered — the stimulus of background may
prove more potent altogether than that of unilateral
light. In such circumstances, C. roscoffensis remains
on the black half of the dish, although the rays
of light signal to it to approach their source. It
looks as though the facts or illusions which, in

4—2

52 PLANT-ANIMALS [OH.

higher animals, are named choice and volition are
illustrated in our plant-animals by the simplest of
working models. If this view is accepted, it would
seem to follow that the intricacy and mystery of
complex habits and instincts are begotten of the
ever-increasing complexity of conditioning or ac-
cessory stimuli which have first attached them-
selves to and then replaced the original series of
stimuli.

Some further facts with respect to the photo-
tropic responses of C. roscoffensis are worthy of a
passing word.

In the first place, just-hatched animals, though
they respond to the directive stimulus of gravity, do
not respond to that of light. After a few hours of
free existence, they acquire the faculty of responding
tropistically to unilateral light, which henceforth be-
comes a masterful factor in determining their habits.

In the second place, the rays of light to which
C. roscoifensis responds tropistically are not those
which induce phototropic curvatures in plants. As
is well known, a plant exposed, unilaterally, to rays
of the less refrangible part of the spectrum — the red
for example — shows no phototropism ; whereas a plant
subjected on one side to blue- violet light reacts as
readily as to white light. Convoluta roscoflfensis, on
the other hand, responds not to blue or violet light,
but to green light. The diagram (Fig. 12) represents

II]

HABITS OF CONVOLUTA

53

Fig. 12. Tropistic reaction of Convoluta roscoffensis to Monochro-
matic Light. Each circle represents a ground-plan of a shallow
porcelain vessel containing a central heap of sand, a little sea-
water, and many Convolutas (represented by dots). The break
in the circle (Series 1) indicates the position of the window in
a blackened bell-jar placed over each porcelain vessel. The
arrows represent the direction of the light. Series 1 shows
the disposition of Convoluta at the time of removal of the
covers. Series 2 shows the instant negative phototropic reaction
set up by removing the covers (raising the light intensity).
Series 3 (only one example shown) shows the recovery (a few
seconds after Series 2) of the positive phototropism. The green
light was produced by passing daylight through three of Baker's
green gelatine films ; the red by using three of Baker's red films ;
the blue by using four of Kirchmann's blue films and one
green film. (The blue and green lights were not absolutely
monochromatic.)

54 PLANT-ANIMALS [OH.

the results of a series of experiments with unilateral,
monochromatic light. As the illustration shows,
the animals — represented by dots — mass themselves
toward the source of light when that light is
white or green. In blue light, they remain distri-
buted with fair uniformity around the periphery of
the containing vessel. In red light they show some
sign of a negative reaction.

The most probable explanation of this re-
sponse to green light is that the orange eye-spots
and pigment glands are the organs of light-per-
ception ; and that the pigment contained in the eye-
spots and glands absorbs principally the green light.
From observations on other animals it would appear
probable that green light not infrequently serves
marine organisms for purposes of perception : nor,
when we reflect upon the green-blue colour of sea-
water, will this appear surprising.

In the third place, C. roscoffensis, with its well-
defined tropisms, is an admirable subject in which to
study what without a great violation of language we
may call the problem of the parallelogram of physio-
logical forces : in other words, the problem of the
mode of response of an organism to two directive
stimuli, simultaneously applied and acting along dif-
ferent lines. As might be expected, when two stimuli
act on C. roscoffensis one not infrequently dominates
the other, so that the resulting reaction is that which

ii] HABITS OF CONVOLUTA 55

would occur were the dominating stimulus alone
applied. This happens, as we have seen, when C.
roscoffensis is subjected to both light- and heat-
stimulation.

So also, in the case of light and gravitational stimuli
acting simultaneously, the mode of response of C.
roscoffensis shows that the latter stimulus may be
ignored.

Thus, if animals are placed in water in a tall
glass cylinder on a steady table, they rise to the
surface of the water and congregate on the side
toward the light. If the light-conditions are modi-
fied by the interposition of a black card or plate
of ground glass between the source of light and the
top of the water, C. roscoffensis relaxes its hold and
swims downward to take up a new position just
below the edge of the screen. Geotropism is sub-
ordinated to phototropism.

Subjected to simultaneous stimulation by light
and gravity, C. roscoffensis behaves exactly like a
green plant placed under similar conditions. Though
the stem of a green plant is negatively geotropic,
yet, if it is illuminated from below, the plant,
ignoring gravitational stimulation, directs the tip of
its stem downwards toward the source of light.

The behaviour of both plant and animal would
seem to indicate that, in the reflex groundwork
of nervous activity, something akin to the pheno-

56 PLANT-ANIMALS [CH.

menon of attention in psychic life may manifest
itself.

Even though he may not be concerned with
problems of reflex action, the biologist who would
investigate the life histories or structure of such
animals as C. roscoffensis must pay some heed
to their tropistic behaviour, for on this knowledge
his successful manipulation of the living animals
depends.

Thus, to obtain plentiful supplies of eggs we may
make effective use of the phototropic reaction. Large
numbers of mature C. roscoffensis are placed near a
window in a flat, glass dish containing sea- water. The
animals move up to the light. At nightfall, the dish
is turned round. The operation, if performed care-
fully, does not disturb the animals. They remain
throughout the night in that part of the vessel which
was nearest the light during the previous day. Cer-
tain of the animals deposit egg-capsules. In the
morning, the animals, responding to the directive
stimulus of light, cross over to the side turned
toward the window. The egg-capsules thus left
behind are readily visible to the eye and may be
picked out by means of a pipette. In this way, several
hundred egg-capsules may be obtained in the course
of a few days.

Again, young C. roscoflensis are so minute that
they may be found only by a practised eye. Never-

ii] HABITS OF CONVOLUTA 57

theless, by exploiting their background reaction, they
may be picked out easily.

By laying a small sheet of white paper on a black
cloth and standing the dish containing the animals
partly on the black and partly on the white ground,
the animals are caused to accumulate above the
latter. There, however, they are almost invisible ;
but by turning the vessel round so that the part
above the white paper is brought over the black
cloth, the animals may be seen distinctly and picked
out by means of a fine pipette before they scuttle
oif again to the white ground. To transfer a young
C. roscoffensis from one vessel to another is difficult
enough till its geotropism is pressed into service, when
the operation becomes quite easy. The animal is lifted
in a pipette ; but on endeavouring to expel it from the
tube by pressing the indiarubber nipple of the pipette,
only the water is discharged, and C. roscoffensis is left
sticking to the side of the glass tube. To avoid this, the
pipette is held vertically and no effort made to eject the
water. The slight, involuntary shaking of the hand
suffices to render the animal negatively geotropic.
Down it swims till it reaches the drop of water at the
point of the pipette, whence the gentlest pressure
suffices to transfer both drop and animal to another
vessel.

So far, this study of the behaviour of our plant-
animals has been confined to the investigation of their

58 PLANT-ANIMALS [OH.

tropistic responses to light and gravity. A stimulus
may however induce responses in an organism of a
very different kind. It may give rise, not to a change
of place, but to a change of state. Such effects of
stimulation are called tonic effects, and the organism
which responds to them is said, to be in a state of
tone or tonus. Certain peculiar effects of this kind
are well known among human beings and may serve
us as illustrations. People who work all day by
artificial light, specially by unmitigated electric or
incandescent gas light become irritable and depressed.
Professional photographers, who spend long hours in
"dark rooms" developing photographs in red light,
suffer mentally in a similar way. The change of
state induced by such abnormal conditions we may
describe as a change of tone. We will assume that
light is indispensable to the human race, that men's
bodies are attuned to light and that this harmony
is maintained by an unceasing sequence of light-
stimuli which contribute to the well-being of the
nervous system. Then, if we adopt this view, it will
be easy to imagine that a cessation of the rain of
stimuli may prejudice the well-being of the nervous
system and be the origin of disorders of more or
less severity.

How far the normal nervous state of human
beings is determined by the tonic effect of light it
is not possible to say ; but there is no doubt that

ii] HABITS OF CONVOLUTA 59

this phototonic effect is of considerable and even
fundamental importance to the well-being of many
animals and plants.

If a green plant is placed in darkness the
mechanism of its growth is thrown out of gear.
Though it grows, and, if supplied with proper food,
might, for all we know, go on living indefinitely, its
nervous state is changed, its tone has been affected.
It becomes " drawn," as gardeners say, its stem grows
long and supple, and its leaves remain small and un-
developed. As, without the controlling baton of the
conductor, the unity of the orchestra is lost, and, it
may be, harmony is replaced by discord, so, without
the constant influence of light, the harmony of growth
which obtains normally throughout the plant is dis-
turbed. Since, therefore, light-stimuli contribute to
the maintenance of the normal nervous state of the
plant, we say that light exerts a tonic influence. In-
asmuch, however, as even in the absence of light
the plant remains alive and capable of some sort
of growth and development, we must conclude that
the state of tone in which it lives is not the result
of light but that it is modified by light. This
effect of light in modifying — to the advantage of the
organism — its state of tone is called phototonus. The
language is clumsy but the ideas which it conveys
are clear enough, though lacking in precision.

C. roscoffensis is, as we know, attuned to a high

60 PLANT-ANIMALS [OH.

light intensity. It exposes itself on the beach to the
bright light of the midday sun with nothing between
it and desiccation but a constant, filmy stream of
salt, drainage-water. In such situations, it retains its
powers of activity unimpaired for hours. If, however,
it is placed in a vessel with some sand and water, taken
to the laboratory and kept in darkness, it passes after
some days into a lethargic condition. In this state
of dark-rigor C. roscoffensis remains on the surface of
the sand and may even fail to respond by downward
migration when subjected to the stimulus of vibration.
So also, after prolonged exposure to high light
intensity, a similar lethargic condition — a light-rigor —
comes over the plant-animals. Even in their natural
positions on the beach, after long hours of exposure
to the sun's glare, colonies of C. roscoffensis may be
observed in which all the members appear to be
overcome by light-rigor. They lie roped together
by the slimy excretion of their skin, inert, floating
in water-puddles. At times, chunks of a colony in this
state may be detached by running water, and small
green masses, each of many thousand individuals, are
borne seaward by the drainage stream. In this
lethargic state of light-rigor, which both young and
old animals exhibit, C. roscoffeusis is difficult to
manipulate ; for example, attempts to transfer them
from one vessel to another by means of a pipette
result generally in damage to the animals. To this

n] HABITS OF OONTOLUTA 61

lethargy or light-rigor — here attributed to exposure
for long periods to high light intensities — is due the
fact that, whereas, on some days, the C. roscoffensis
patches on the shore disappear before the water of
the making tide reaches them, yet, on other days,
the multitude of animals composing a patch lies
motionless and indifferent to the approach of the in-
coming tide. Not till the first wave sweeps over them,
do the animals throw oif their sloth and disappear.

We have now to attempt to apply the knowledge
we have obtained of the tropistic responses of C.
roscoifensis to light and gravity, and of the tonic
effects of light, to the elucidation of the most strikingly
picturesque feature of the behaviour of this animal,
that of its tidal uprising and downlying. Almost as
soon as the water of the falling tide has run off the
roscoffensis zone, the green colonies appear, and,
before the making tide invades it, they vanish. The
purposes of ascent and descent are obvious. By its
ascent, the animal reaches the light without which —
for reasons we shall discover subsequently — it cannot
live; by its descent, C. roscoffensis maintains its
situation on the shore and escapes the waves.

As our study of its tropisms makes clear, these
movements of ascent and descent may be induced in
the laboratory by subjecting the animals to appro-
priate stimulation. Vibrations produced by tapping

62 PLANT-ANIMALS [CH.

the sand or the containing vessels send them down,
only to reappear when the tapping has ceased. But,
as we have seen, a colony may disappear before the
tide has mounted high enough to disturb it. The
eyes of C. roscoffensis — mere pigment spots — are too
rudimentary to allow us to suppose that it sees the
water coming in and so takes warning and descends
betimes. Indeed a simple experiment suffices to
demonstrate, not only that this is not the case, but
also that whole colonies of C. roscoffensis may descend
beneath the sand in the total absence of an apparent
external stimulus.

Thus, if a batch of animals from a roscoffensis patch
is scooped up with sand and water by means of a cup
and taken into the laboratory, the shaking to which, of
necessity, the specimens are subjected in the process
causes their swift descent. By the time the cup is
brought indoors, not a trace of green may be visible
in it ; but, in the calm of the laboratory, the animals
reascend once more and lie as a thick, dark green
scum upon the surface of the sand. They remain in
this state for hours, then suddenly disappear.,

Wondering at this swift retreat, and as we wonder,
staring through the laboratory window at the shore
a stone's throw away, we note first vaguely and then
with quickening curiosity that the rising tide is just
about to flood the roscoffensis zone. Curious, this
descent of the green scum of animals in the cup !

ii] HABITS OF CONVOLUTA 63

Some hours elapse, and, as the tide is running off
the roscoffensis zone, curiosity, or its after-effect,
provokes us to inspect the cup on the laboratory
table. Even as we look into it, a faint green colour
steals over the surface of the sand, and, in a minute
or two, it is almost black with a dark crowd of
C. roscoffensis. Now curiosity joins with astonish-
ment to beget a new idea. More cups are found
that the observation may be repeated and coincidence
put out of court. Each time we repeat the observation
on fresh batches of animals we obtain the same result.
As on the shore in the roscoffensis zone, so in the
laboratory the upward and downward movements of
Convolute march with the movements of the tide. As
the tide recedes from their home upon the shore, the
sojourners in the laboratory rise up : as the tide rises
over it, they sink down. In the absence of all apparent
external stimulus, C. roscoffensis, obedient to its
custom, yet keeps time with the tide. The rhythm of
the tides is reflected by the movements of the animal.
For eight successive tides (Fig. 13) the animals in the
laboratory maintain their rhythm, synchronous with
the ebb and flow of the waters over the roscoffensis
zone : then, though the rhythmic movement up and
down may yet continue, its temporal periodicity
loses precision, and, finally, the rhythm is worn down.
This stage reached, the animals exchange a working
day of double, six-hour shifts, two up, two down, for

64

PLANT-ANIMALS

[CH.

one of a single, twelve-hour spell of " upness " with a
like twelve-hour spell of " downness." In other words
they phototrope themselves up to the light as day
breaks and sink down with the sun.

Whence comes the power whereby C. roscoffensis
acts as a tide-indicator? What orders its rhythmic
coming and going?

Onth*
Short

Ligkt

Fig. 13. The rhythmic tidal movements of C. roscoffensis. The
curves represent the rise and fall of the tide. The horizontal
lines included within the tidal curve indicate the "up" or
"down" positions assumed by the animals. "In Laby. light"
shows that, with animals kept in the laboratory and exposed to
light during the day, the rhythm is lost after seven or eight
periodic tidal movements up or down. "Light agitated" shows
that animals exposed to constant vibration lose their periodicity
more quickly. " Dark " that in constant darkness periodicity does
not manifest itself.

A French biologist, Dr Bohn (1903), who has
also observed this periodicity of upward and down-
ward movement, rejects the view which is put forward

n] HABITS OF CONVOLUTA 65

below, and regards the phenomenon as a manifestation
on the part of C. roscoffensis of " memory of the shock
of the waves." Certainly, if all other explanations fail
— if we can discover no agent which serves to jog this
memory — we must accept this suggestion ; though in
doing so, it might be well to ask ourselves whether it
is to be regarded as an explanation or as a succinct
statement of our ignorance.

Experimental investigation of the phenomenon
would appear to indicate that no such large demand
on memory — or mneme — as that which is implicit in
the above hypothesis need be made.

In the first place, as we have noted already,
C. roscoffensis does not remain on the surface of
the sand at night. Hence we must suppose, on the
memory hypothesis, either that it forgets to arise from
the dark sand when it is dark on the surface, or that
it remembers, rises, and finding nothing better to do,
goes to bed again.

The behaviour of C. roscoffensis in constant dark-
ness is yet more difficult of interpretation on this
hypothesis. For, when kept in continuous dark-
ness, C. roscoffensis ceases to exhibit periodicity of
alternate up and down movement. There may be
one movement downward and one upward ; but, after
that, the animals remain upon the surface of the
sand day after day until they die (Fig. 13).

Again, if the downward movement is due to a

K. 5

66 PLANT-ANIMALS [CH.

memory of past vibrations caused by the making
tides invading periodically the C. roscoffensis zone,
how much more certain should be the effects of
present vibrations. Yet, if the vessel containing the
animals is so exposed that a steady drip of water falls
upon the surface of the sand contained in the vessel,
C. roscoffensis clings to its periodic habit. As soon as it
perceives the vibrations it descends and remains below
the sand. When, however, the time for its uprising
arrives, it rises to the surface, and, in spite of injuries,
remains upon the surface. It seems difficult of belief
that the memory of a particular kind of blow can be
a more powerful spur to action than the actual
receipt of an unceasing series of blows of a like kind.
The original suggestion which, though it is not ac-
cepted by the author of the memory hypothesis,
seems to fit the facts, seeks to explain the periodicity
of upward and downward movement exhibited by C.
roscoffensis by connecting it with tonic light effect.

In support of this it may be mentioned that
C. roscoffensis fails to exhibit its tidal rhythm except
when it is subjected to a fairly high light intensity
during its period of " upuess." Thus, even in a room
at some little distance from the window, the movement
does not keep tidal time.

Again, other observations indicate that the spell
of illumination counts for something in determining
the precision of the movements. Thus, if three

n] HABITS OF CONVOLUTA 67

batches of C. roscoffensis, collected directly after
the colonies emerge, are put in darkness for periods
of one, two, and three hours respectively, and are
then exposed to the light, that which had only one
hour's run in darkness descends first, and that which
had two hours' darkness descends next.

Taking the results of these experiments into con-
sideration and bearing in mind the condition of
lethargy which C. roscoifensis may manifest, in its
natural station, after long light-exposures, we are led
to frame some such hypothesis as the following, in
order to account for the periodic tidal movements
exhibited by this animal.

Phototropism and background reaction lead C.
roscoifensis to the most illuminated parts of that
region of the beach which provides it with a con-
tinuous, filmy stream of water.

Independently of its tropistic effect, light exerts
a tonic effect on the physiological state of the
animals. Under the combined influences of tropistic
and tonic light-stimuli, C. roscoffensis is held — at
attention — in the "up" position : in other words, whilst
subject to this constant rain of phototonic stimuli, it
remains negatively geotropic. True, if the sand is
agitated, the vibrations set up suffice to change the
sign of its response to gravity and send it geotroping.
Nevertheless it is easy to show that the response of
C. roscoffensis to the vibration- stimulus is less marked

5—2

68 PLANT-ANIMALS [OH.

at the beginning of an " up " phase than it is toward
the end of that phase. Thus, if specimens are col-
lected as soon as the tide is off the colonies and are
brought in a vessel into the laboratory, they swarm
up to the surface almost as soon as the vessel ceases
to be shaken, whereas animals collected after a long
light-exposure and placed in a similar position, may
remain down till the next tidal " up " phase is due.

Thus it is reasonable to conclude that, after some
five or six hours of light-stimulation, internal changes
are induced which act as stimuli and cause the animal
to change the sign of its response to gravity. It
becomes positively geotropic and descends beneath
the sand. In the darkness of the sand, recovery of the
original, normal state takes place gradually, and the
animals now respond to the stimulus of gravity by
a movement in the opposite sense. They ascend to
the surface. In its simplest form, the hypothesis
involves the assumption that prolonged light-exposure
and prolonged dark-exposure modify the tone or state
of nervous irritability of the animals, and that these
changed conditions manifest themselves by a changed
mode of response to gravitational stimulus. After
a prolonged light-exposure, the animals are positively
geotropic ; after a corresponding sojourn in the dark,
they become negatively geotropic. The reversal of
the direction of a tropistic movement is by no means
unusual among plants and animals. Thus, in order

n] HABITS OF CONVOLUTA 69

to cause horizontally growing lateral roots to take up
vertical positions, it suffices merely to remove the
main root. As a result of the operation, the physio-
logical state of the whole root-system is so changed
that members formerly transversely geotropic become
positively geotropic, and tertiary roots which previous
to the operation were ageotropic (non-geotropic) and
hence grew indifferently in any direction, become
transversely geotropic.

Similar changes in sign of tropistic response
may be induced by definite changes in the environ-
ment. For example, as Loeb has pointed out, fresh-
water Copepods, (small Crustacea) taken from the
same pond at the same time, may exhibit, some a
positive, some a negative, phototropic response and
others may be non-phototropic. If, however, a little
carbon-dioxide is added to the water they all become
positively phototropic. It is not improbable that this
uniform migration of the animals in the direction of
the light which follows on the addition of carbon-
dioxide is an example of response to associated
stimuli. Copepods feed no doubt on algse, which
can only live and grow in the light. In the course of
their nutrition, algse decompose carbon-dioxide and
liberate oxygen, so that the amount of carbon-dioxide
contained in the water in their immediate neigh-
bourhood is less than that contained in the darker
regions of the pond. Much carbon-dioxide will be

70 PLANT-ANIMALS [CH.

correlated with limited food supply. Now it has
been shown definitely in the case of other animals,
e.g. the caterpillars of Porthesia, that they are only
positively phototropic so long as they are not fed.
If this holds good for Copepods, their response to
increased carbon-dioxide becomes at once intelligible
on the mneme or associated stimulus hypothesis.
Thus hunger affects the tone or physiological state in
such a way that the Copepods respond to light by
directive movements whereby food supplies become
available. The movement brings the animals from a
part of the water which contains a maximal amount
of carbon-dioxide to a part where, thanks to the
presence and activity of the green algse, — the food
sought by the Copepods — the water is not fully
saturated with carbon-dioxide. When the animal
encounters carbon-dioxide conditions which are
normally associated with hunger conditions, it takes
the hint and photo tropes just as though it were
hungry. For a hungry man, a cook-shop window has
an irresistible attraction, whereas to the well-fed
person it may offer no seduction, or even be
repulsive : nevertheless, " si par impossible " the
odour which emanates from it is very agreeable, the
well-fed may deign to sniff.

What internal changes, chemical or other, resulting
from the prolonged light-exposure of C. roscoffensis
on the beach, give the signal for its dismissal from

ii] HABITS OF CONVOLUTA 71

the attitude of attention which it takes up during
the " up " period we do not know. Nor may we say
with confidence that the explanation of the periodic
rhythm which we have offered is complete or final.
The subject deserves more detailed study than it has
yet received, both for its own sake and for the light
which it may throw on the origin of habit and, it
may be, also, of instinct.

PART II

THE NATURE OF THE PLANT-ANIMALS

CHAPTER III

THE GREEN CELLS OF CONVOLUTA ROSCOFFENSIS
AND THE PART THEY PLAY IN THE ECONOMY
OF THE PLANT-ANIMAL.

IT is not only on account of their behaviour, as
exhibited by the tropistic movements and periodic
phenomena which we have recorded, that the plant-
animals C. roscoflensis and C. paradoxa attract the
attention of the biologist. The most superficial
microscopic examination is sufficient to convince
him that their tissues are not like those of other
animals. The green cells of C. roscoffensis and
the yellow-brown cells of C. paradoxa arrest his
attention. In regular and close rows, just beneath
the surface, of the body, lie the green cells of
C. roscoifensis, each so minute as to be invisible to
the unaided eye and yet so numerous as to be the
source of the dark, spinach-green colour of the
animals (Frontispiece and Fig. 14). Though less
numerous and less regularly arranged, the yellow-
brown cells which lie beneath the skin of C. paradoxa
are, like the green cells of the former species, striking

76

PLANT-ANIMALS

[CH.

and puzzling objects (Frontispiece and Fig. 15).
Puzzling because, whilst they seem to be just as
much integral parts of the bodies of the animals as
any other tissue-elements, they have nevertheless
a foreign and plant-like appearance. So plant-like

OT-.

Diat*

Fig. 14. A young Convoluta roscoffensis. GC = green cells. Diat.
and R = remains of diatoms ingested and digested. OT = otocyst.

indeed is the aspect of C. roscoffensis as seen under
the microscope, that a botanist might well be excused
for mistaking it for a fragment of a leaf, endowed
with an uncanny kind of movement.

in] GREEN CELLS OF CONVOLUTA 77

In yet another and no less remarkable way,
C. roscoffensis exhibits a plant-like character. The
bodies of normal, mature animals never contain the
slightest trace of food-substances. Though it is
kept for days in pure sea-water till any ordinary
marine animal would be ravenous, — in point of
fact most marine animals are always ravenous — an
adult C. roscoffensis makes no attempt to ingest any

Y.B

YB.

Fig. 15. The superficial tissues of Convoluta paradoxa.
Y.B.= yellow- brown cells.

food-substances which may be added to the water.
Though tempted with diatoms, green algse, starch
grains, oil drops, milk, or lamp-black, it remains with
its capacious mouth so pursed up as to be invisible
and refuses to ingest any solid food whatever. Till
last year it seemed that there was no exception to
this fasting habit of adult C. roscoffensis ; but during

78 PLANT-ANIMALS [CH.

observations on animals which had been kept for a
month in darkness in pure sea- water, certain individuals
were discovered which had so far condescended from
this ascetic mode of life as to have become cannibals.
Instead of being straight and slim, they carried a
large pouch-like distension about the middle of their
bodies. Microscopic examination showed that the
pouch was occupied by another adult Convoluta as
large as that which had engulfed it. Hence it follows
that normal adult C. roscoffensis in its natural state
does not refrain from food because it cannot swallow,
but because it does not want to eat.

Now green plants do not take up solid food : they
manufacture it. From inorganic substances, water
and carbon-dioxide, which are absorbed from without,
the green cells of plants manufacture sugar. This pro-
cess, which is a preliminary to nutrition, is termed by
botanists, photosynthesis, since the energy required
for the manufacture of the carbohydrate (sugar) is
derived from the radiant energy of light. The
green pigment, chlorophyll, which is associated
in the green cells of the plant with specialised,
granular bodies called chloroplasts, absorbs light,
and in some way, as yet imperfectly understood, this
radiant energy is utilized by the protoplasm of the
chloroplasts in the manufacture of sugar. The plant
possesses also the power of synthesising yet more
complex substances. Beside carbohydrates such

in] GREEN CELLS OF CONVOLUTA 79

as sugar, which consists of carbon, hydrogen and
oxygen, the plant prepares synthetically its own
nitrogenous food-substances, the proteins. Though
next to nothing is known of the details of protein-
synthesis as carried on by the plant, this much is
known, that the nitrogen contained in the proteins
is derived by the green plant from inorganic sources,
chiefly from nitrates which are absorbed in solution
from the soil or water in which the plant is growing.
Having thus manufactured its food-substances from
raw, inorganic materials, the plant is free to feed
upon them, that is, to use them either to build up
and repair its living substance (protoplasm) or to
convert them directly or indirectly into substances
(secretions) which enter into the composition of its
tissues. Thus, for example, from the photosynthesised
carbohydrate, are derived the cellulose substances
which form the enclosing shell or cell-wall within
which is contained each individual mass of protoplasm
which we call a cell or protoplast. But beside serving
such constructive purposes, much of the manufactured
food-substance, particularly the carbohydrate material,
is used for respiratory purposes, that is, for supplying
the energy wherewith the plant does the work of
living. By inducing compounds like sugar to unite
with oxygen, their decomposition and oxidation are
effected, with the result that energy is liberated and
simpler substances, e.g. carbon-dioxide and water, are

80 PLANT-ANIMALS [OH.

produced. The liberated energy serves for the per-
formance of the work which the living plant must do,
and also, converted into heat, contributes to maintain
the temperature of the plant's tissues at a proper
level. The surplus of carbohydrate and of protein
not used for constructive or respiratory purposes the
plant puts by for future use. The starch, oil and
nitrogenous substances contained in seeds, tubers,
and other storage-organs of plants represent this
reserve food-material.

The power possessed by the green plant of manu-
facturing food-materials in excess of its immediate
needs is the lever which makes the whole world of
animal life to move. For the animal has no such
synthetic powers, and yet it requires the same food-
substances as the plant. Hence it is constrained to
take them from the plant. The aphorism "all flesh
is grass" is no mere figure of speech, but a terse
statement of truth.

Though the foregoing facts are, of course, the
commonplaces of plant-physiology, yet they require
mention here, for it follows from them that, if C. ros-
coffensis does not take in solid food, it must either
absorb it in solution or manufacture food for itself.
Since the plant-animals not only live very well but also
increase and multiply in pure sea-water, and since pure
sea-water contains but the merest traces of any organic
substances which might serve them as food, we are

in] GREEN CELLS OF CONVOLUTA 81

driven to accept the latter alternative, and to conceive
of C. roscoffensis as an animal which lives like a plant,
in other words, as a plant-animal. This conclusion
forces us to direct our attention to the plant-like
green cells which form such a prominent tissue in
the body of C. roscoffensis.

From the general considerations which we have
just advanced, it would appear to follow that the green
cells possess the power, common to those of green
plants, of manufacturing carbohydrate food-materials
from the simple, inorganic, soluble substances, water
and carbon-dioxide, and possibly also of manufacturing
complex nitrogen-containing food-substances, such as
proteins, from simpler bodies. If we succeed in
proving that the green cells of C. roscoffensis possess
these powers, other problems will present themselves.
Thus, we shall want to know, what are the green
cells? Is C. roscoffensis born with them or does it
acquire them ? If it acquires them, how do they get
into the body and what are they like before they
become constituents of the body of the animal ?

As a preliminary to the investigation of these and
other problems on the origin, significance and fate of
the green cells, we will turn back to consider further
the behaviour of C. roscoffensis and C. paradoxa with
respect to food. The various observers who have
occupied themselves with investigations into the
mode of life of C. roscoffensis have all reached the

K. 6

82 PLANT-ANIMALS [CH.

conclusion that this animal does not take up solid food.
A similar apparent total abstinence has been recorded
in cases of other animals which contain green or
yellow cells not unlike those which occur in our
plant-animals. Thus no food has been seen in the
bodies of certain adult Radiolaria, Ciliata, Hydro-
corallines and Madreporaria, and in all these animals
from which remains of food are absent, coloured cells
are present. Hence the natural inference has been
drawn that such animals subsist on the food-materials
manufactured synthetically by their green or yellow
cells.

If, however, the evidence which we have now to
bring forward with respect to C. roscoflensis is
applicable to the other green- or yellow- celled
animals, then, though the conclusion may contain
a large measure of truth, the premise on which that
conclusion is based is erroneous.

When referring to the abstemious habit of
C. roscoffensis we were careful to state that it is the
mature animal which does not take up solid food.
As a matter of fact, from the time of hatching to
the period of maturity, C. roscoffensis feeds, and
feeds voraciously. Indeed, its catholicity of taste
is remarkable. Diatoms, unicellular algee, spores of
various kinds and, in the absence of more nutritious
substances, grains of sand are swallowed with avidity
(cf. Fig. 14). Arrived at maturity, it ceases to ingest

in] GREEN CELLS OF CONVOLUTA 83

solid food-substances. As old age comes on, it begins
to feed upon its green cells. Groups of such cells in
all stages of digestion and varying in colour from
yellowish-green to brown may be seen lying in large
vacuoles in the central digestive tissue of the bodies
of old specimens of C. roscoffensis. Thus, though,
as we shall see presently, the green cells of C. ros-
coffensis play an all-important part in the economy
of that organism, they are not the sole purveyors of
nourishment to it. Throughout a considerable part
of its life, C. roscoffensis is able to help itself to the
solid food supplied by the micro-flora and fauna of
its environment.

Unlike C. roscoffensis, its ally, C. paradoxa, knows
no abstemious fits. Throughout its life it is a glutton.
A glance at the body of the larval animal (Fig. 16)
gives the impression of a marine museum, so accom-
modating is the body of C. paradoxa. There, may
be seen the remains of several scores of diatoms of all
shapes and sizes. When examined immediately after
capture, a young or old C. paradoxa may be found to
contain, not only diatoms, but two or three Copepods,
each half as large as the animal itself, and, if it be late
in the summer, rows of tetraspores of red algse show
through the transparent body like so many cardinal
buttons. In C. paradoxa therefore, as in C. roscoffen-
sis, though the coloured, plant-like cells may well
play an important and even indispensable part in the

6—2

84

PLANT-ANIMALS

[CH.

life of the animal, they are not called upon to cater
for all the food that it requires.

As a first step toward the investigation of their
origin and rdle, we will make a microscopic examina-
tion of the coloured cells of our plant-animals.

--YB

Fig. 16. A larval Convoluta paradoxa showing cilia and bristle-like

projections from skin. YB = the only yellow-brown cell contained

in the body. M= mouth and gullet. OC = eye spots. OT = otocyst.

The tissue of the body is crowded with large numbers of

diatoms which have been ingested.

When a living C. roscofFensis is examined under
the low power of the microscope, its green cells are
seen to be, some spherical, some pear-shaped and

in] GREEN CELLS OF CONVOLUTA 85

some of irregular form. As the animal moves along,
its muscles contract and the shapes of the green cells
change somewhat (cf. Fig. 14). Seen under a higher
power, the green cells present the appearances indi-
cated in Fig. 17. Each cell or protoplast is made
up of a large green, and a small colourless part.
The former consists of the chloroplast, the latter of

F:G.

Fig. 17. Cross- section of the superficial tissues of Convoluta roscoffen-
sis. G .C. = green cells in rows. N = nucleus of green cell. Py r =
pyrenoid. Mes.C.=r nucleus of attendant cell. F.G. = fat granules.
CM = cilia at the surface of the animal. Ep = epidermis.

colourless protoplasm. Embedded in the mass of
colourless protoplasm, but not visible without special
methods of preparation, is a denser, oval body, the
nucleus which is an integral part of plant and animal
cells. Lying in the chloroplast is a dense body sur-
rounded, halo-like, by a clearer margin. This body,
which is called a pyrenoid, consists of proteins and is

86 PLANT-ANIMALS [CH.

characteristic of the cells of many of the lower algse
(Fig. 21, p. 123).

If a green cell is treated with a solution of iodine,
the nucleus and the pyrenoid are stained brown, and
round the latter a thin, blue, granular layer may be
distinguished. This layer is known as the starch
sheath. As the action of the iodine continues,
minute, lens-shaped starch grains — distinguished by
their blue colour — may be seen lying in the chloro-
plast. Unlike algal cells in general, the green cells
in the body of C. roscoffensis have no cellulose wall,
but are bounded each by an elastic layer of protoplasm.

The yellow-brown cells of C. paradoxa are built
on somewhat different lines. Each cell contains a
number of irregularly oval, or polygonal, yellow-
brown, discoidal chloroplasts which occupy about
half of the cell (Fig. 18). The other half of the yellow-
brown cell consists of clear, transparent, vacuolated
protoplasm. By suitable treatment, involving the
dissolution of the pigment, a nucleus may be made
out, slung in the centre of the cell by threads of
protoplasm which stretch from the periphery. When
the cells are treated with alcohol, the yellow-brown
pigment is dissolved away and green chlorophyll,
previously screened by the yellow-brown pigment, is
seen in the chloroplasts. The reaction is useful in
that it enables us to distinguish the chloroplasts
of the yellow-brown cells from the orange-coloured

in] GREEN CELLS OF CONVOLUTA 87

glands which occur in the surface-tissues of the body
of the animal.

The green pigment of C. roscoffensis is chlorophyll,
identical in its spectroscopic properties with that
contained in the green tissues of plants. Moreover,

Fig. 18. Yellow-brown cells of Convoluta paradoxa. I. As seen in an
animal some hours after capture. II. As seen immediately after
capture. The spherical masses lying in the cells and also outside
them represent the fat-globules referred to on pp. 89 and 91.

The shaded oval bodies at the periphery of the cells represent
chloroplasts.

as Geddes (1879) has demonstrated, the green cells
of C. roscoffensis are capable of photosynthesis. When
the animals are exposed to light, they decompose
carbon-dioxide, give off oxygen, and manufacture
carbohydrates, the excess of which is stored in the
chloroplast in the form of starch.

That the starch which occurs in the green cells

88 PLANT-ANIMALS [CH.

of C. roscoffensis owes its origin to photosynthesis, we
demonstrate by the method which is used for a similar
purpose in the case of plants. The living animals
are kept in darkness and examined daily for starch.
After a time — about seven or eight days in young
C. roscoffensis, about fourteen days in older animals—
when, as indicated by the samples tested, starch has
disappeared — having been converted into sugar and
used as food or in respiration — the animals are
brought into the light and tested at intervals for
starch. As is the case with green plants treated
similarly, photosynthesis is resumed as soon as light
falls on the green cells, and within less than ten
minutes starch, which represents the reserve form of
the photosynthesised carbohydrate, makes its appear-
ance in the green cells. Moreover, the light which
is most efficient for photosynthesis in plants, that of
the red end of the spectrum, is also most efficient for
photosynthesis in the green cells of the plant-animal.

It is not so easy to obtain rigid proof that the
yellow-brown cells of C. paradoxa are capable of
photosynthesis. Nevertheless, the indirect evidence
supports strongly the view that they do actually
function in this manner.

In the first place, like similarly coloured alga3,
Avhich are known to manufacture their food photo-
synthetically, they possess a screening pigment and
also chlorophyll.

in] GREEN CELLS OF CONVOLUTA 89

In the second place, when examined immediately
after capture, the transparent reticulum of the cells
(Fig. 18, n) is found to contain colourless, refractive
globules or droplets, which, when treated with suit-
able reagents (osmic acid, etc.), may be recognised to
consist of, or at all events to contain, fat. Now, it
is well known that certain plants, some algse among
others, store their reserve, photosynthesised carbon-
compounds, not as starch, but as oil. That these
globules are of the nature of reserve substances
derived from the products of photosynthetic activity
is rendered probable by the following facts. First,
when a catch of animals is divided into two lots, and
one is kept in darkness and the other in the light, the
reserve fat-globules disappear more quickly from the
yellow-brown cells of the dark-kept animals than
from those of the animals kept in the light. Second,
if two similar batches of animals are kept in darkness,
one in pure (filtered) sea-water, the other in sea-water
containing sea- weed from the C. paradoxa zone, fat
disappears from both, but more quickly from the
yellow-brown cells of the starved animals. If the
fat were derived from the food (sea-weed with its
micro-flora and fauna) there would seem to be no
reason why it should disappear at all from the yellow-
brown cells of the fed animals. On the other hand,
assuming that the fat-globules serve as food-material,
not only for the yellow-brown cells but also for those

90 PLANT-ANIMALS [CH.

of the animals, we should expect that the latter, when
deprived of other supplies, would make larger de-
mands on the reserve fat of the yellow-brown cells
than when the animals had access to other food
supplies. Third, if C. paradoxa are kept in filtered
sea-water, and hence deprived of all food except that
which it can obtain from the yellow-brown cells,
then, so long as they are exposed to the light, the
yellow-brown cells continue to contain fat-globules.
Since animals deprived of food get just as hungry
in the light as in darkness, it would appear to follow
that the reason why the fat does not disappear from
the yellow-brown cells of the light-kept animals is
that, as fast as it is removed to serve for the nutrition
of the animal, it is reformed by the yellow-brown
cells. It is therefore to be concluded that the fat-
globules are reserve products of the photosynthetic
activity of the yellow-brown cells.

Thus we reach a definite stage in the course
of our enquiry into the significance of the green
and yellow-brown cells of C. roscoffensis and C.
paradoxa. These cells are capable, in the same way
as the chlorophyll-containing cells of plants, of manu-
facturing organic, carbon-containing substances from
inorganic materials and of storing the surplus in the
form of starch or fat.

Our next step must be to determine whether the
products of the photosynthetic activity of the coloured

in] GREEN CELLS OF CONVOLUTA 91

cells are available for the nutrition of the tissues of
the animals which contain them.

The evidence which suffices to demonstrate that
the coloured cells do actually make contributions to
the nutrition of the animals is not far to seek. If
C. paradoxa is examined microscopically immediately
after capture, it is seen that the tissues of animals
whose yellow-brown cells are rich in droplets of
reserve fat contain also large numbers of globules
of a similar nature (Fig. 18). Moreover, the appear-
ance of the fat-globules contained in the yellow-
brown cells suggests most forcibly that the fat lying
in the tissues of the animal owes its origin to the
secretion of fat by the yellow-brown cells. The
appearance of the yellow-brown cells recalls, in this
respect, that of cells of a mammary gland in its active
stage. Just as the fat contained in the milk which
is secreted by the cells of a mammary gland is
liberated in droplets by the rupture of the clear
vacuolated parts of the secreting cells, so droplets
may be seen in course of extrusion from the yellow-
brown cells into the tissues of the animals (Fig. 18).
The large, clear, anterior end of the yellow-brown
cell — only to be seen in fresh-caught animals which
have been exposed in their natural habitat to a fairly
high light intensity — contains often one, large fat-
globule. In some yellow-brown cells, one or more
droplets lie in the deeper part of the clear anterior

92 PLANT-ANIMALS [OH.

end, whilst, in others, a single, large drop lies close
against the anterior margin of the cell, separated
from the tissues of the animal only by the thinnest
of membranes. Finally, other large globules may
be seen lying just outside the colourless borders of
yellow-brown cells and presenting the appearance
of having been extruded from them. We conclude
that the fat-globules, formed in the yellow-brown
cells of C. paradoxa, pass by a process of secretion
from these cells to those of the animal and serve the
animal for nutritive purposes.

It is very probable that a similar secretion occurs
in C. roscoffensis. For, in the first place, starch,
which, as we have learned, appears in the green
cells as the result of photosynthesis, does not occur
in the other tissues of C. roscoffeusis. In the second
place, this animal does not possess the power of
digesting starch. When supplied with starch grains,
it ingests them readily, transfers them to the
vacuoles which lie in its digestive tract, but is
unable to dissolve them. They remain for a time
in the vacuoles, and are then discharged by a
temporary rupture of the surface of the body.
In the third place, in carefully prepared and
stained sections through the body of C. roscofiensis,
there may be seen rows of fatty granules passing
from the green cells to the neighbouring animal
cells (Fig. 17, F.G.). Nor does a conversion of

in] GREEN CELLS OF CONVOLUTA 93

starch into fat present any difficulty to vegetable
cells. For example, in many trees, the tissues of the
trunks contain, in autumn, large stores of starch ; as
winter advances the starch is replaced by oil or fat,
and, again, when spring arrives, the oil is recon-
verted into starch. It is of course open to us to
suppose that, just as the sugar formed photosyn-
thetically by the green cells of a leaf is translocated
as fast as may be through the tissues of the leaf-stalk
and stem to meet the demands of the colourless cells
of the plant which depend for their food supplies on
the activity of the green cells, and just as the starch
which appears in the green cells of the leaf represents
only the surplus which is stored temporarily in a
convenient form to be changed to sugar and dis-
tributed later on ; so, in C. roscoffensis, the photo-
synthesised sugar streams away as such to the
colourless cells of the animal, only the surplus
being stored as starch.

Whether it travels as sugar or, as the former
observations seem to indicate, as fat, there is no
doubt that the organic, carbon-containing food-
material, produced photosynthetically by the green
cells of C. roscoffensis, serves for the nutrition of the
animal's tissues.

Indeed, as we show presently, unless the green
cells are present in the body of the animal, and
unless they increase and multiply therein, the animal
does not grow at all.

94 PLANT-ANIMALS [CH.

The phase in the relation between coloured,
chlorophyll-containing cells and animal tissues which
we have just described, presents the closest parallel
with the relation which obtains between the green
and non-green cells of any chlorophyllous plant.
In both plant and plant-animals, the chlorophyll-
containing cells manufacture carbohydrates in excess
of their own requirements, and, in both, the excess is
translocated to the colourless tissues and used by
them as food-material.

But, in certain circumstances, C. paradoxa and,
to a somewhat less degree, C. roscoffensis may exploit
their coloured cells in a more summary manner.

Thus, when animals are kept in darkness in sea-
water filtered through a Pasteur-Chamberland filter
they become reduced greatly in size. The reduction
in size is, as we know, greater, and takes place more
rapidly, in dark-kept than in light-kept animals.
In one experiment in which the animals were
measured, those which had been kept in darkness
were, on the average, two and a half times as small
as those which had been kept in the light; the
average superficial dimensions of the dark-kept
C. paradoxa being "08 square inch and those of
the light-kept animals *2 square inch.

The powers of resistance to starvation of both
C. roscoffensis and C. paradoxa are extraordinary.
Thus, it is possible to maintain C. paradoxa alive for

m] GREEN CELLS OF CONVOLUTA 95

upwards of a month in filtered water ; that is, under
conditions, in which it is deprived of all external
supplies of food. When subjected for long periods
to these conditions, the animals become reduced in
size and — as is the case to a yet more marked degree
with those kept in darkness — also show an extra-
ordinary reduction both in number and size of their
yellow-brown cells.

In prolonged darkness, the yellow-brown cells, once
their reserves of food-material have been extracted
from them to meet the needs of the animal, are
digested wholesale by C. paradoxa. If the water in
which they are contained is altogether devoid of food
supplies, the attack by the animal on its coloured
cells occurs all the sooner. Even in the light, if
external food supplies are withheld from C. para-
doxa, a time comes when, although the yellow-brown
cells are supplying it with photosynthesised food-
materials as fast as they can under the difficult
circumstances, it turns upon them ; — killing and
digesting the goose which laid its golden eggs.

Microscopic examination of animals kept in pro-
longed darkness supplies evidence that the degenera-
tion of the yellow-brown cells is not a mere decay
within the body, but is the result of a true process
of digestion exerted on them by the animal. The
first sign of digestive action is a reduction in size
of the yellow-brown cells. They assume a more

96 PLANT-ANIMALS [OH.

spherical shape and their chloroplasts become smaller
and rounder. Each reduced algal cell is now seen
to lie in a distinct, digestive vacuole containing a
pink fluid. Next, the pigment of the chloroplasts is
dissolved and, diffusing out of the cell, may impart a
brown colour to the vacuolar fluid. At this stage,
the chloroplasts are greenish ; later, they become
colourless. Finally, heaps of few or many, colourless,
curiously persistent granules are all that remain of
the algal cells.

It is interesting to observe, in this connection, that
if animals are brought, after a prolonged sojourn in
darkness, into the light and supplied with fresh
sea- water, yellow-brown cells make their appearance
again in their bodies. As they grow and increase
in numbers, the animals also begin again to grow.

So also in the case of C. roscoffensis, if the green
cells fail to make their appearance in the body, the
animals remain of microscopic size. If, on the other
hand, the green cells appear, increase and multiply
to form the characteristic green tissue, the animals
begin to grow rapidly.

Thus in various ways it has been demonstrated
that C. roscoffensis and C. paradoxa depend for
their food on their coloured cells. Without them,
they fail to grow. When, by exposure to dark-
ness, the coloured cells are put out of photosyn-
thetic action, the animals become reduced in size,

in] GREEN CELLS OF CONVOLUTA 97

and, after giving their coloured cells a respite
of some weeks, they turn on these algal cells and
digest them. In C. paradoxa, this raiding of the
coloured cells occurs only under special, artificial
conditions ; as, for instance, during prolonged dark-
ness. But, in the case of C. roscoffensis, it is a regular
procedure with animals which have reached a certain
age. Nor is the reason for this difference of be-
haviour between the two plant-animals far to seek.
Whereas C. paradoxa retains its habit of ingesting
solid food and looks to its yellow-brown cells for sup-
plementary supplies only, C. roscoffensis, at a certain
stage, shuts its mouth and cultivates its garden of
green cells. Now, inasmuch as hunger — cell-hunger
— may be due to one or more of many different
lacks, lack of carbohydrate, lack of nitrogenous food-
substances, or of mineral compounds, it is bound to
happen sooner or later that the animal part of C.
roscoffensis, in its phase of total abstinence from
food, will feel the pinch of one kind of hunger or
another. Goaded by this all-powerful stimulus it
turns upon its green cells, and, biting the hand that
fed it, seeks, by devouring them, to satisfy its cravings
for some special food-substances.

To the question what particular kind of hunger
is it that drives the animal to devour its plant-like
cells, we shall address ourselves, after we have in-
vestigated, in the next chapter, the origin of these

K. 7

98 PLANT-ANIMALS [OH.

cells. For the present, we content ourselves with
summing up what we have learned of the relations
between the animals and their plant-like cells.

The coloured cells manufacture photosynthetically
food-materials, storing the surplus as starch and fat.
The animal receives from the coloured cells supplies
of food-material. So plentiful are these supplies in
C. roscoffensis that the animal comes, in course of
time, to rely altogether upon them for its nutrition.
Ceasing to take up food, it grows, bears eggs, and
produces young at the expense of the materials
supplied by its green cells. This life of curious
asceticism leads, however, to trouble. Though the
green cells continue to supply organic carbon com-
pounds, something or other is lacking from the
prepared food which the animal thus receives. To
make up for this lack, it digests in detail its green
cells, coming often in old age to present a strange
appearance — head-end green, tail-end white. Hav-
ing exhausted its stores of green cells, without
apparently satisfying all its needs, it pines away
and dies.

In its earlier youth, C. roscoffensis feeds, after the
manner of animals in general, on other plants or
animals. This is the first phase. In the course thereof,
green cells appear in the body, increase, multiply,
photosynthesise and distribute food materials to the
animal's tissues. For a while, C. roscoffensis receives

in] GREEN CELLS OF CONVOLUTA 99

food from two sources — from ingested plants and
animals and from its green cells.

This second phase is succeeded by a third, in
which C. roscoffensis, having ceased to ingest solid
food, is nourished, in the same manner as the colour-
less non-chlorophyllous tissues of a green plant are
nourished, by the products of the photosynthetic
activity of its green cells.

Last stage of all which ends this strange eventful
history: — the animal digests its green cells, and,
having done so, dies.

In the first phase, the mode of nutrition is
animal-wise : in the second, part animal-, part plant-
wise : in the third, altogether plant- wise or holo-
phytic : and in the fourth, autotrophic, that is by
living on itself.

Convoluta paradoxa is like unto C. roscoffensis,
except that its experiments in nutrition stop, under
normal circumstances, at phase two. Under artificial
conditions, however, it behaves like its ally, lives for
a while like a plant at the expense of the products
of photosynthesis of its yellow-brown cells, and,
finally, driven to digest these cells, prolongs its life
autotrophically.

7—2

CHAPTER IV

THE ORIGIN AND NATURE OF THE GREEN CELLS
OF CONVOLUTA ROSCOFFENSIS.

GREEN, yellow or brown cells, resembling in a
general way those contained in the bodies of C. ros-
coffensis and C. paradoxa, are found in many different
kinds of animals belonging to the lower groups of the
animal kingdom.

Such cells are known to exist in representatives
of every division of the free-living Protozoa — the
lowest group of animals. They occur in certain
sponges, in many sea-anemones and in various
species of coral-forming animals. In higher groups,
they are rare though they are known to occur in
isolated cases, for example, in Zoobothrium, a
member of the Polyzoa, in Elysia (a Mollusc), and
in Echinocardium (an Echinoderm).

The best known example of an animal containing
green alga-like cells is the common, freshwater hydra,
Hydra viridis.

In certain of the animals which are characterised
by the possession of coloured cells, these peculiar

CH. iv] GREEN CELLS OF CONVOLUTA 101

elements are invariably present. In other animals,
the coloured cells may occur in some individuals,
but not in others. The former, general association
we may call obligate, and the latter, occasional
association, facultative.

Hydra viridis, Convoluta roscoffensis and C.
paradoxa are examples of organisms in which the
association is obligate.

facultative association may take one of two
forms. Either some specimens living in a given
region may possess coloured cells, whilst other speci-
mens of the same region lack them, or a given
species may consist, in one part of its range, of
individuals all of which contain coloured cells, and,
in another part of its range, of individuals none of
which possess them. For example, Noctiluca is colour-
less in the North Atlantic, but green in the Indian
Ocean. British Alcyonium have no chlorophyll-
containing cells, whereas the nearly allied Alcyonium
ceylonicum possesses them. It seems probable — and
this is a point of which we shall make use presently—
that association between animal and plant-like cells
is commoner in the warmer than in the colder seas.

The problem of the origin and nature of the green,
yellow and brown cells which occur in animals has
engaged, from time to time, the attention of zoologists.
Long ago the name Zoochlorella was given to the green
cell and Zooxanthella to the brown or yellow-brown

102 PLANT-ANIMALS [OH.

cell. Since, however, these names are applied, re-
spectively, to any green and any brown plant-like
cell which occur in any animal their value is but
limited.

That Zoochlorellse and Zooxanthellse are plant-
like cells is undisputed. They contain chlorophyll,
decompose carbon-dioxide with evolution of oxygen,
may, in the case of Zoochlorellse, contain starch : a
substance for the manufacture of which plants and
not animals possess the secret. Further, in some
cases, at all events, the coloured cells possess a wall
of cellulose, another substance the formation of
which is confined exclusively or almost exclusively
to members of the vegetable kingdom.

Beside one or more chloroplasts, a nucleus and
a pyrenoid, the coloured cells have been shown in
some cases to contain a small, bright red body known
as an eye-spot (Fig. 21, p. 123). In free-living, uni-
cellular algse, the eye-spot serves the purpose of light-
perception and thus is part of the nervous machinery
for the performance of phototropic movements. Hence
its occurrence in green cells imprisoned in the bodies
of animals may be regarded as a strong indication
that the green cell which possesses it had once a
free-living existence.

Nevertheless, though such facts as these lend
powerful support to the hypothesis that Zoochlorellse
and Zooxanthellse are algal cells which have aban-

iv] GREEN CELLS OF CONVOLUTA 103

doned their free and independent modes of life and
have taken up their abodes in the tissues of animals,
yet they do not constitute a final proof of the truth
of this hypothesis. Indeed, the problems presented
by the chlorophyllous cells of animals are too
numerous and important to be dismissed by means
of a loosely-drawn inference of this sort. To the
possession of chlorophyll the plant owes its powers
of photosynthetic manufacture ; and to the absence of
this pigment from the cells of animals is due the
dependence of the animal world on the world of
plants for food supplies. Yet, low down in the
animal kingdom, organisms exist which, though un-
doubtedly possessed of distinct animal characteristics,
contain chlorophyll and use it for the manufacture
of carbohydrate food. Thus, species of Euglena
(e.g. E. viridis), which stand near the parting of the
ways which lead, the one to the animal kingdom,
the other to the vegetable kingdom, contain chloro-
phyll and use it for photosynthetic purposes. Now
Euglena viridis is undoubtedly an animal. The single
cell or protoplast of which it consists is provided
with a gullet, into which solid particles may pass
and thus be ingested by the animal. The membrane
which encloses the organism is not composed of
cellulose — the cell-wall substance of typically vege-
table organisms ; and in yet other ways Euglena
gives evidence of its "animal" nature.

104 PLANT-ANIMALS [OH.

Although zoologists and botanists are agreed that
the genus Euglena belongs to the animal kingdom,
yet it possesses the power of constructing a green
pigment — chlorophyll — which is identical in physical
properties with that which occurs in the chloroplasts
of plants. Here there is no question, apparently, of
any swallowing by Euglena of plant cells. The
animal cell makes the pigment in the same way as
a plant cell makes it, and, having made it, uses it
for photosynthetic purposes.

In certain circumstances, chlorophyll disappears
from the body and Euglena viridis passes into a colour-
less phase. When in this state the animal, if it is to
feed at all, must do so by ingesting ready-made food.
That is, from being a holophytic organism — one with
a typically plant-like mode of nutrition — it becomes
heterotrophic, that is, it feeds on ready-made, organic
materials, obtained from its environment. After a
time, it may reconstruct its chlorophyll and become
free once more to manufacture by photosynthesis its
organic food-substances from the raw, inorganic
materials of its environment.

If one species of animal can do this, why should
not other, even more highly developed species,
possess like powers ? Why should there not appear,
here and there, animals which resume the habit
possessed by their ancestors, construct chlorophyll and
become independent, photosynthesising organisms ?

iv] GREEN CELLS OF CONVOLUTA 105

Or, to pursue another line of argument. The
Zoochlorellse of some animals are typically plant-like
cells. They possess a chloroplast, a nucleus and a
cellulose cell-wall. But in other animals, in C. ros-
coffensis, for example, the green bodies are of simpler
build. Each consists of a naked protoplast which is
made up of a green chloroplast and a colourless mass
of eccentrically lying protoplasm in which a nucleus
may be included (Fig. 17, p. 85). The green tissue,
composed of vast numbers of these elements, appears
to be as much a part of the animal as any other of its
tissues. So much is this the case that all attempts to
cultivate the green cells of C. roscoffensis outside the
body end in failure. They are no more capable of inde-
pendent existence than are the chloroplasts of the
chlorophyllous tissues of a green plant.

What is there to prevent us from assuming, as
Haberlandt has assumed, that the green cells of C.
roscoffensis are not complete cells but merely chloro-
plasts, and that, like the chloroplasts of the green plant,
they are transmitted as colourless particles (leuco-
plasts) from the organism to its eggs, and, multiplying
as the egg divides to form the embryo, reappear as
green chloroplasts in the tissues of the new genera-
tion ? On this hypothesis the colourless part of the
green cell of C. roscoffensis (Fig. 17) is an animal cell
which attends upon the green chloroplast. In other
words, just as a green cell of a flowering plant

106 PLANT-ANIMALS [CH.

consists of colourless, nucleated protoplasm contain-
ing chloroplasts, so, on Haberlandt's hypothesis, the
green cell of C. roscoffensis consists of a colourless,
animal part containing a green chloroplast.

Pursuing this hypothesis to its natural conclusion,
it is easy to imagine, with Haberlandt, that, in some
remote past, algal cells came to exist in symbiosis
with colourless C. roscoffensis ; that the animal offered
such a congenial lodging as to induce the algse to give
up going out altogether. They abandoned their cell-
wall as an enclosing apparatus no longer of service
to them. In return for security and all the comforts
of a home the green cells prepared the food both for
themselves and for their host. Submitting itself to
the guidance of the animal, the green cell aban-
doned its nucleus and became reduced to a naked
chloroplast.

So it might have come about that the only powers
retained by this relic of a once complete and free
algal cell are those possessed by the chloroplast of
a green plant, namely, the powers of photosynthesis
and of division to form new chloroplasts. Moreover,
just as the chloroplasts contained in the egg-cells of
plants lose their green pigment, and become colourless
leucoplasts, which, dividing as the cells of the plant-
embryo divide, give rise to the chloroplasts of the
next generation, so, on this hypothesis, it would follow
that the green chloroplasts of C. roscoffensis might

iv] GREEN CELLS OF CONVOLUTA 107

give rise to colourless leucoplasts which pass into
the egg and provide the rudiments from which the
chloroplasts of the larval animal are developed.

Yet again, if this were indeed the course of events
in C. roscoffensis, if, from their free, complete con-
dition, the original green cells which gained access
to the body of our plant-animal have become reduced
to mere chloroplasts, might not this animal provide an f
illustration of the mode of origin of the higher green
plants themselves ? In a remote past, a symbiosis
was struck up between a colourless organism and
a green alga — such a communal mode of life, for
example, as that presented by lichens at the present
day. Convenient models these to show us the
relation between colourless organism and undoubted
algal cells. So happy is the hypothetical partnership
between alga and colourless organism that new
developments ensue. A new and composite form of
life comes into existence. The colourless tissues
burrow in the earth and supply, along well-defined
conduits, the water and minerals required by the
green cells. They form tall trunks and spreading
branches to lift the chloroplasts — the representatives
of the algal cells — nearer to the sun. The green plant
is in being.

Of this alluring picture, evoked by syren-voiced
hypothesis, we are bound to ask the simple, sober
question, is it true? To this question we can give

108 PLANT-ANIMALS [CH.

no answer until we have discovered experimentally
the origin of the plant-like cells occurring in each
species of the many animals which possess them.

This we proceed to do in the case of C. roscoifensis.
Two methods are open to us for the purpose. We must
either trace back the green cells to the earliest stage
at which they make their appearance in the animal
and ascertain whether they may be then identified
with any known, free-living alga. If we succeed in
this, we shall have obtained, not absolute proof, but
strong ground for believing that the green cells are
of intrusive origin. Or — and this is the only certain
way — we must cultivate the alga, and having ob-
tained animals which are free from it, and having
demonstrated that such animals remain indefinitely
colourless, we must infect the animal with the algse
of our pure algal-culture and synthesise the green
plant-animal.

As we have indicated already, all attempts to
isolate living green cells from the body of C. ros-
coffensis have failed ; and so it would seem that the
former, less satisfactory method alone remains. The
application of the method is simple enough. It
consists in the microscopic examination of larval
C. roscoffensis in all stages, from the time of hatch-
ing up to the time when green cells, resembling those
of the adult, may be recognised within the body.

iv] GREEN CELLS OF CONVOLUTA 109

When just-hatched C. roscoffensis are examined with
the high power of the microscope, no green cells are
to be seen in their bodies, nor are there present any
colourless cells resembling in shape or structure the
green cells, nor do either eggs or larvae appear to
contain leucoplasts.

If just-hatched animals are transferred to sea-
water filtered by means of a Pasteur-Chamberland
filter, though, in the course of time, some may become
green, many remain colourless. Therefore it is highly
probable that the green cells do not owe their origin
to^colouflesTantecedents (leucoplasts) present in the
eggs7~For7were such forerunners of the green chloro-
plasts present, they would develop into chloroplasts
in all, or at all events in the great majority, of the
larvae. On the other hand, if young animals are
hatched and allowed to remain in ordinary unfiltered
sea-water, green cells make their appearance with
certainty in the animals in the course of one or two
days. In the youngest larvae, there are to be seen
no more than two or four green cells, each of them
lying in a clear vacuole and occupying a fairly definite
situation in the body. Two such cells lie right and
left, a little behind the otocyst and two right and
left about the middle of the body. By their repeated
division is produced ultimately the whole contingent
of green cells of the adult body.

At stages earlier than this, no green cells are to

110 PLANT-ANIMALS [OH.

be found, but a larger or smaller, colourless body may
be seen lying in a central vacuole in such a situation
as to suggest that it has been taken up through the
mouth. The larger body consists of two closely
opposed cells, the smaller of a single cell. In
either case, the colourless body is surrounded by a
mucilaginous wall which swells considerably as its
contents divide, in the case of the single cell into
four, in that of the large cell, into eight daughter
cells. The colourless cells, each about 15 to 16 /JL in
length (= about jg1^ inch), are discharged by the
bursting of the vacuole and take up positions similar
to those in which the four green cells are found.
Though colourless and of granular content, a large,
oily looking pyrenoid may be made out in each cell (cf.
Fig. 22, B, Pyr., p. 125), and by appropriate methods
of staining, the presence of a nucleus may be demon-
strated. The colourless cells increase in size and, in
each, a red eye-spot makes its appearance as a little,
lateral patch near the margin. Soon a distinction is
to be seen between a colourless plug of protoplasm
and a cup-shaped, granular mass which occupies the
major part of the cell (Fig. 22 (7). A faint yellow
colour steals over the cup-shaped, granular mass, the
yellow colour deepens and, becoming green, enables
us to identify the cup-shaped, granular mass as a
chloroplast. The cell, now a green cell, possesses no
cell- wall, and differs only from a green cell of an adult

iv] GREEN CELLS OF CONVOLUTA 111

C. roscoffensis in its more regular, oval shape and in
the possession of an eye-spot. Each green cell divides.
The daughter cells formed by the division lack the
oval shapes of the mother cell : they lack also eye-
spots. The colourless plug or neck of protoplasm no
longer occupies the position of a cork in a flask, but
lies eccentrically to the chloroplast and in it the
cell-nucleus is contained. In short, they are identical
with the green cells of the adult animal. Thus we
reach two conclusions of importance. First, that the /
green_cells of C. roscoflensis are preceded by colour-
less cells. Second, that thejnass o:f colourless proto- 2
plasm attached to the green cell is not, as Haberlandt
suggests, an animal cell standing in close relation
with a chloroplast, but is an integral part of the
green cell. As the young green cell continues to
divide, a significant change may be observed in the
shape and state of the nucleus. Distinct and spheri-
cal in the colourless and original green cells, it becomes,
in the cells produced by successive divisions, more
granular and indistinct, till, when the number of
green cells has increased considerably, some only
among them may be seen to contain nuclear material
—fine granules in a clear area : the rest contain no
trace of nuclear material. In other words, the great
majority of the green cells of the adult animal are
not complete cells, but cells which show all stages
of diminishing nuclear substance (Fig. 17). Inasmuch

112 PLANT- ANIMALS [CH.

as it is a well-established fact that the nuclear part
of the protoplasm plays an important role in the
life and work of the cell, these observations throw
light on the subordination of the green-celled tissue of
C. roscoffensis to that of the animal. Since, also, the
nucleus is known to play a part in cell-wall formation,
we are no longer surprised that a cell- wall fails to
form in the green cells. Further, in this progressive
nuclear degeneration, we have the explanation of the
inability of the green cells to survive separation from
the tissues of the animal. Those green cells whose
nuclei are least degenerate are capable of division,
but even they have suffered. They are no longer
able to form a cell-wall nor to exist as independent
organisms. As division succeeds division, the nuclear
material becomes further reduced till, in the adult
animal, it is often difficult to find any sign of nucleus
in the large majority of the green cells.

It is highly probable that the advent of this
enucleate stage in the green cells is the signal to
the animal to devour them. Though still capable
of photosynthesising, the green cells, unable to offer
resistance to those of the animal, are surrounded by
the latter, devoured and digested. A significant
phenomenon is revealed by the drawings (Fig. 17) of
sections through the green cells of C. roscoffensis.
In places, ingrowing rows of cells may be seen budded
off from the outermost green cell and, of these rows,

iv] GREEN CELLS OF GWVOLUTA 113

only the outermost contain a distinct nucleus, others
possess deep-staining granules, and others no nuclear
material whatever. A parallel suggests itself between
the green cells of C. roscoffensis and the red blood-
corpuscles of the higher vertebrates. As the red
discs are enucleate, partial cells budded oif from the
nucleated red cells, so may the green cells be regarded
as enucleate, partial cells budded oif from the outer-
most, nucleated green cells ; and, as the red blood cor-
puscles are of limited life and specialised (respiratory)
function, so are the green cells of C. roscoffensis of
limited life and of specialised (photosynthetic)
function.

The green cell, devoid of nucleus, would not,
however, appear to be shut off from all nuclear
influences. For the enucleate green cell may be
connected by fine processes with another green cell
still possessed of nuclear substance (Fig. 17, p. 85).
Moreover, such green cells as are without nuclear
material are accompanied by a large attendant nucleus
of animal origin. This close association of " attendant
nucleus" and green cell is shown in Fig. 17, Mes.C.
It may be that the attendant nuclei are those of
"wandering cells" of the animal which lie in wait
for enucleate green cells and, at a subsequent stage,
digest them.

The astonishing closeness of the relationship
between animal and green cells offers some support

K. 8

114 PLANT-ANIMALS [OH.

for the hypothesis, suggested independently by
Schimper and Lankester, which we have already
outlined as to the composite nature of higher green
plants. The algal cells of C. roscoffensis are on
the road which leads to complete loss of inde-
pendence. In the higher green plant this loss is
complete. The green cells of C. roscoffensis lose
cell-wall and nucleus, but retain some colourless
protoplasm ; the green elements of the flowering
plant — if they are regarded as the descendants of
originally free algse — have lost everything except the
photosynthesising organs — the chloroplasts.

But a wide gap remains between the state of
affairs in C. roscoffensis and that in the higher green
plant. Sooner or later C. roscoffensis destroys and
digests its green cells, and none of them, nor any
colourless representatives of the green cells, pass into
the egg-cells ; whereas the higher green plants pro-
vide for the future crop of chloroplasts in their
descendants by transmitting colourless rudiments of
the chloroplasts to their egg-cells.

An adult C. roscoffensis is a complex of two
organisms — one, the colourless animal, the other, the
chloroplast-remainders of the original, green, nucle-
ated, algal cells. In its case, unlike that just imagined
for the green plant, the synthesis is not a permanent
one. It endures but for the lifetime of the animal
and has to be recommenced in every larval Convoluta.

iv] GREEN CELLS OF CONVOLUTA 115

The discovery that the green cells of C. roscoffensis
arise, in the larval animal, from a colourless cell
which lies in a vacuole near the mouth of the animal,
makes it all but certain that they are of extraneous
origin, and that, in the course of ingesting solid food,
the larvse take up also these antecedents of the green
cells.

Failing the isolation and cultivation of the green
cells, and failing the discovery of the colourless
or green cells in the sea-water, all that seemed pos-
sible to do more was to demonstrate that animals
hatched in pure, filtered sea-water, remain colour-
less. The method adopted for this purpose was as
follows. Large numbers of animals were scooped up
in a watch-glass as free from sand as possible. They
were brought into the laboratory, allowed to geotrope
into a white cup and washed repeatedly with filtered
sea- water. Their habit of sticking to the surface of
the cup after it had been tapped gently, permitted
of the water being poured off without any consider-
able loss of animals. After washing them many
times, the animals were transferred to filtered sea-
water in large glass dishes. In due season, the egg-
capsules were formed and since, though very minute,
they are visible readily to the practised eye, they
could be picked out and transferred yet again to
filtered sea-water. In this they were allowed to
hatch. Though the results of such experiments,

8—2

116 PLANT-ANIMALS [OH.

which were repeated many times, confirmed the
infection-hypothesis they were not sufficiently uni-
form to establish it absolutely. Time after time, the
minute larvse showed, when examined microscopic-
ally, a general absence both of green cells and colour-
less precursors of green cells ; but, time after time,
also, an occasional animal reared under these ap-
parently sterile conditions was found to contain
green cells. Though the occurrence of green cells
among animals hatched in filtered sea-water was
infrequent and sporadic, yet there such animals were
and, to make matters worse, the longer the larvee
were kept under observation, the larger was the
number of specimens which contained green cells.

Evidently, either the infection-hypothesis was
wrong or there was some defect in the experiment.
A careful examination of the conditions of the ex-
periment revealed ultimately a source of error and
opened up the possibility of a new origin for the
green cells. The mucilaginous capsules, enclosing
groups of eggs, were discovered to be infested with
all sorts of minute organisms. On the capsules, and
in them, were many different kinds of microscopic
animals and plants — diatoms, infusoria and forms of
life unlike any to be seen elsewhere. Since the egg-
capsule is formed by a secretion of the skin, and since
the skin of the animal is covered with slime, it was at
once clear that repeated washing in filtered sea- water

iv] i GREEN CELLS OF CONVOLUTA 117

had not succeeded in making the animals biologically
clean. It was clear, also, that, if the infecting organism
came from the egg-capsule, it might be derived not
from the sea- water but from the body of the parent.
At the time of hatching, there might be liberated
from the body of the animal, colourless or green
cells which, though they could not live in sea- water
and were not to be cultivated artificially, might well
be capable of living in the walls of, or inside, the
egg-capsules.

Fortunately, the elimination of this source of
error though laborious is not impossible. When
ready to hatch, a very little help suffices to enable
the young to escape, not only from the thin mem-
brane which encloses each, but also from the common,
mucilaginous egg-capsule. Thus, by drawing a clutch
into a small pipette and then ejecting it and the water
from the pipette, the capsule bursts and the young
escape. In this way, it was possible to separate
larvse from their capsule-remnants. By employing
this method, large numbers of larvse, white, minute
and active, were isolated in filtered sea-water in
which the only source of infection lay in such in-
visible shreds of the capsule as might have happened
to get themselves transferred with the larvse to the
filtered sea-water.

The method proved successful. In one case, out of
forty-four larvae isolated from capsule-remnants and

118 PLANT- ANIMALS [CH.

kept under observation for nearly three weeks, only
five animals contained green cells. In another case,
not a single animal of a total of forty-seven was
found to contain any trace of green cell or colourless
precursor.

Further, on transferring such uninfected animals
to ordinary, unfiltered sea- water, they became uni-
formly green in the course of one or two days.

We conclude therefore that the green cells of
C. roscoffensis are algae ; that the species to which
they belong exists as a free-living, independent,
marine plant; that this alga has a colourless stage,
as well as a green stage, in its life-history ; that the
alga lives on the egg-capsule as well as in sea-water ;
that it is ingested with the food, and, resisting
digestion, is planted in the body where it increases
and multiplies and forms the green tissue of adult
C. roscoffensis.

The questions remain : What is this alga and what
does it look like in its free stage?

All sorts of attempts, some ludicrous in their
extravagance, were made to isolate the infecting
organism ; whilst all the time it was lying under the
eye. None of the attempts succeeded, and, during the
winter, when experimental work could not be carried
on, there was nothing to do but to contemplate rue-
fully the note-books recording the failures. But some
wise person once observed, " You learn to play cricket

iv] GREEN CELLS OF CONVOLUTA 119

during the winter and to skate during the summer " ;
— a paradox which contains a biological truth, for
the effects of exercise sum themselves up and write
the addition in our experience, not during the exer-
cises, but in the intervals between them. At all
events, it was in the winter that a scrutiny of results
of the previous summer's work showed that when
green animals appeared among larvse left with their
capsules in filtered sea-water, the manner of their
appearance was like that in which an epidemic
declares itself. At first, it marks down a single
victim, then some of the neighbours are affected till,
by and by, the disease is general. So it was with
the green-cell infection of C. roscoffensis. For
days after animals hatched in sea- water had become
quite green, those hatched from capsules kept in
filtered sea-water remained colourless. Then one
green, among many non-green, appeared. The
numbers of green animals increased, till, finally,
all became green. At once the conclusion presents
itself. In our experiments, the colourless stage of
the Iarva3, which lasts as long as fourteen days, is an
incubation period, not for the animal but for the
infecting organism. Here or there, in spite of many
washings, a single algal cell which had settled on
the surface of the body has remained entangled in
the slime covering the animal. Transferred during
egg-laying to the capsule, it grows and divides. It

120 PLANT-ANIMALS [OH.

increases till it forms a multitude. Then the capsule
bursts and swarms of infecting organisms are liberated
and, ingested eagerly by C. roscoffensis, give rise to
the chlorophyllous cells of its body. The idea sug-
gests the simple method : isolate the empty capsules,
as well as the just-hatched young, and in a week or
two some of the capsules will be found teeming with
the infecting organism.

On returning to Brittany in the following summer
the first thing done was to test the hypothesis.
Animals were washed and put to lay in filtered
sea- water ; the egg-capsules were washed likewise and,
when the larvse were hatching out, the latter were
put in one vessel and the remains of their capsules
in another. The animals remained colourless, though,
when samples of them were put into ordinary sea-
water, green cells made their appearance in their
bodies with uniform regularity. After seventeen
days, several small, green, globular bodies, each as
large as a big pin's head, made their appearance in the
water of the vessel containing the capsule-remnants
(Fig. 19). Their hue was the dark spinach-green of
C. roscoffensis. On microscopic examination, under
the slight pressure of a cover-glass, the dark green
mass dissolved and formed a cloud of active, green
flagellated cells, emerging from an egg-capsule (Fig. 20).
Though these free cells differed in various details from
the green cells which occur in the body of C. roscoflen-

iv] GREEN CELLS OF CONVOLUTA 121

sis, it was evident at once that they represented a
stage in the life history of the infecting organism.

Fig. 19. Egg-capsule of Convoluta roscoffensis occupied by a dark
mass consisting of vast numbers of the "infecting organism."
(Magnified forty times.)

The final proof was applied. To the vessel contain-
ing colourless, uninfected Convolutas, some of the
free, green cells were added. Within two days all

Fig. 20. The capsule shown in Fig. 19 enlarged and compressed
during microscopic examination : the ' ' infecting organism "
escaping.

122 PLANT-ANIMALS [CH.

the animals were green. The synthesis of the plant-
animal had been effected. As the result of introducing
an undoubted green alga to a colourless, larval C.
roscoffensis, a green plant-animal was formed.

Since a similar last stage has not been reached in
the case of C. paradoxa — though to reach that stage
is but a matter of time and experiment — we will
devote ourselves not to a description of the incomplete
evidence of its infection by a yellow-brown algal
cell (see Keeble, 1908), but to a continuation of
the study of the life-history of the infecting organism
of C. roscoffensis. The securing of material for this
purpose is comparatively easy once the art of culti-
vating the organism on the egg-capsules has been
learned. It is facilitated also by the fact that the
motile, green cells are, like C. roscoffensis, positively
phototropic and assume, in a vessel of sea-water
exposed to unilateral light, a position identical with
that taken up by C. roscoffensis. Thus, though each
algal cell is far too small to be visible to the unaided
eye, the green, motile cells aggregated together at
the surface of the water on the side toward the light
become collectively visible as a green scum at or just
above the water-line. The fact that they react to
light by a vertically upward movement as well as
by a movement toward the source of light suggests
that the pyrenoid (Fig. 21), a dense blob of protein
surrounded by protoplasm, may perform for the green

iv] GREEN CELLS OF CONVOLUTA 123

cell a function similar to that which the otocyst
performs for the animal. Just as the granule of chalk
which is contained in the otocyst serves, by its gravi-
tational movements, to stimulate C. roscoffensis to
orientate itself, so may the pyrenoid, falling now this
way and now that, serve to stimulate the protoplasm

A

Fig. 21. The infecting organism — an alga belonging to the Chlamy-
domonadineae — seen under the high power of the microscope.
A^macrocyte. B = microcyte. C h I. = chloroplast (represented by
a reticulurn) occupying the greater part of the cell. Nuc.=
nucleus. St. = eye-spot, indicated in A, but not in B, in which,
however, it occupies a similar position. Pyr. = pyrenoid. The
four long threadlike projections represent the flagella.

of the green cell to perform like movements of
orientation.

If the green cells which have taken up their
position along the water-line are examined micro-
scopically, they are found to include many which are
in active movement. Each such cell resembles, in

124 PLANT-ANIMALS [CH.

essentials, the first green cells which appear in the
body of C. roscoflfensis. The bulk of the cell (Fig. 21)
is occupied by a flask-shaped chloroplast (Chi.) in the
middle of which lies the pyrenoid surrounded by its
starch sheath. In the "neck" of the flask-shaped
cell lies a colourless plug or core of protoplasm in
which the nucleus is suspended. On one side of the
chloroplast, a red eye-spot is placed (St.). So far, the
description of the active cell corresponds exactly
with that of one of the first green cells to be seen
in the body of the infected animal. But, in addition
to these structures, two others are met with in the
free, active green cell which are absent from the
green cells contained in the body of C. roscoflfensis.
These new structures are flagella and cell- wall.

The flagella (Fig. 21) consist of four equal, delicate
protoplasmic threads each about twice as long as the
green cell. They project from the anterior end of
the colourless plug of protoplasm, and by their active,
contractile movements serve to row the animal
through the water. The cell- wall which invests the
alga is extremely delicate and gives, when treated
with appropriate reagents, the reaction not of cellulose
but of chitin.

The flagellated cells are remarkable in that they oc-
cur in two sizes (Fig. 21). (The large green cells — macro-
cytes — are about twice as big as the small microcytes.
Such a difference in size occurs not infrequently among
unicellular green algse, and in cases where it occurs it

iv] GREEN CELLS OF CONVOLUTA 125

has been shown that the macrocytes and microcytes
fuse in pairs. As a result of this fusion, a single cell
(or zygote) is produced, which, after passing through
a period of rest, gives rise by division to four or more
daughter cells. Since a similar fusion of two cells
(or gametes) is the essential characteristic of sexual re-
production in all plants and animals, this fusion may be
regarded as a process of sexual reproduction. Under
ordinary circumstances, however, the macrocytes and

Nuc.

C

D

Fig. 22. A = Kesting cell (green or colourless) of the infecting
organism. B = Colourless cell dividing to form daughter cells.
C = Resting cell containing four daughter cells. D = Eesting
cell with eight daughter cells (six shown). Nuc. = nucleus.
Pyr. = Pyrenoid.

microcytes of the infecting organism do not fuse with
one another.

Other cells taken from the green streak along
the water-line possess no flagella (Fig. 22). They
have settled down, withdrawn these structures
and have surrounded themselves each with a thick

126 PLANT-ANIMALS [OH.

wall of mucilage. So rapidly may the wall form
about the encysting green cell, that individuals are
sometimes observed in which the flagella may be
seen in undulating movement within the enclosing wall.

The resting cells (Fig. 22) vary remarkably both
in form and behaviour. Thus, a single, flagellated cell
may come to rest, surround itself with a thin wall
and divide longitudinally into two or four daughter
cells. Each daughter cell, at first naked, organises a
delicate cell-wall, develops flagella and escapes from
the deliquescent mother wall as an active, flagellated
cell. Or an active cell comes to rest, surrounds itself
with a thick wall, takes on a spherical shape and
becomes uniformly green (Fig. 22, A). From such cells
the pyrenoid and eye-spot disappear. Within each
such resting cell, four daughter cells arise, develop
flagella and escape (Fig. 22, (7).

A third form of resting cell occurs (Fig. 22, A).
It is identical with that just described, except that
it is colourless. Like its green counterpart it may
divide to form four colourless daughter cells, which
may be extruded from the mother cell- wall or divide
yet further (Fig. 22, B, C, and D).

Again, paired resting cells occur. Two active
green cells settle down together, become pressed
against one another, and surround themselves with
a common envelope. Such paired resting cells are
either green or colourless.

iv] GREEN CELLS OF CONVOLUTA 127

The existence of paired and single colourless
resting cells formed by the infecting organism in
its free state completes the evidence as to the
identity of this alga with the green cells of C. ros-
coffensis. For, as we have seen, though the alga
may be ingested in its green, flagellated stage,
the more usual mode of infection is by means of
a colourless cell surrounded by a thick wall. This
cell, lying in the central vacuole, undergoes division
into daughter cells, which escape subsequently from
the mother wall and are sown about the body of
C. roscoffensis. The cell originally taken into the
body may be paired or single. In the former
case it gives rise to eight, in the latter case,
to four daughter cells. We conclude, therefore,
that the alga which is the infecting organism of
C. roscoflensis, lives a double life. At times, it has
the form of a green cell, at others, of a colourless
cell. As a green cell it is holophytic, that is it manu-
factures photosynthetically its food materials. As_a
colourless cell it is a saprophyte, feeding like an
animal on ready-made organic material. In its
active stage, it is green and seeks the light : in its
passive stage, it may be colourless and may live in
darkness. Beneath the sand, therefore, where C.
roscoffensis is born, abound vast numbers of the
colourless infecting organism. On its emergence
from the egg-membrane, the larva encounters them

128 PLANT-ANIMALS [OH.

in plenty, lying and dividing on its egg-capsule and
on any other organic debris. Should it escape in-
fection— a rare contingency — C. roscoffensis may, as
we have learned, return to the egg-capsule and thus
incur it. Or, becoming positively phototropic, the
larva moves up to the light. There, at the upper
edges of the water-films, it finds assembled the green,
flagellated organism. Beset in darkness and in light
by the infecting organism, swallowing eagerly all the
minute particles that come its way, C. roscoffensis
cannot escape its destiny. A colourless or green
cell is taken into the body and the plant-animal is
formed.

So pleomorphic is the infecting organism that it
occurs in yet other forms beside those described
already. It may give rise by repeated divisions to
groups of rounded cells lying together in a colony.
Such a colonial form is known as a palmella stage
and occurs in the life histories of various green
algse. It is remarkable that a colourless palmella
form also exists. At any moment, a green member
of the palmella may slip its mucilaginous coat and
appear as a flagellated, active cell.

As to the name and position in the plant kingdom
of the infecting organism we need say but little. Its
characteristics are those of a group of primitive,
green algse know as the Chlamydomonadinese. Like
the infecting organism, the members of this group

iv] GREEN CELLS OF CONVOLUTA 129

are unicellular, bear flagella of equal length and store
their reserve food-material in the form of starch ;
they possess each an eye-spot, a pyrenoid and a cup-
shaped chloroplast, enclosing a core of colourless,
nucleated protoplasm. The only important respect in
which the infecting organism differs from a typical
chlamydomonadine cell is that, whereas the cell- wall
of the latter consists of cellulose, that of the former
has not given in our hands the reactions indicative
of this substance.

Carteria, a genus of the Chlamydomonadinese is
characterised by the possession of four flagella, and
so also is one species of Chlamydomonas (C. multifilis).
Therefore the infecting organism should perhaps be
referred to one or other of these genera. Or it may
be that it belongs to a yet lower group. These are
matters, however, for the systematist to decide.

What is certain is that the green cells of the body
of C. roscoffensis once saw independent days, and
that, for those cells, naked and deprived of nuclear
material, these independent days are gone never to
recur.

K.

CHAPTEE V

THE SIGNIFICANCE OF THE RELATION BETWEEN
COLOURED CELL- AND ANIMAL-CONSTITUENTS
OF THE PLANT-ANIMALS.

WE have discovered enough already, with respect
to the relations which obtain between algal cells and
animals in our composite plant-animals, C. roscoffensis
and C. paradoxa, to convince ourselves that the re-
lation is not one of casual intimacy, lightly entered
upon and lightly abandoned ; but one which is of
fundamental importance to the animals. Before it
was realised how vital was this association, we
entertained hopes of raising a colourless race of
C. roscoifensis, and, having done so, of comparing
the colourless with the green adult, with the purpose
of ascertaining what changes had arisen in the
organism as the result of the symbiosis. Though
this hope has not been fulfilled, though it has proved
a task, if not impossible, yet beyond our powers,
nevertheless the attempts to accomplish it have
brought to light facts which show how ingrained in the
lives of the worms is this habit of association with
the algal cells of their respective infecting organisms.

CH. v] NATURE OF PLANT-ANIMALS 131

The attempts have also provided us with informa-
tion with respect to the full significance of the
association. In order to make clear the nature of
this information, we will first consider very briefly
the normal course of events in the development of
C. roscoffensis in ordinary sea- water containing the
infecting organism and then its behaviour in filtered
sea- water which contains no infecting organisms.

Within a day or two of hatching, C. roscoffensis,
maintained in ordinary sea-water, is found to have
become infected. The colourless cell, the first sign of
infection, divides and the colourless daughter cells are
sown about the body. They become green, divide and
re-divide till ultimately the many thousands of algal
cells making up the green tissues of the organism, lie
in dense masses in the body. For a time, the animal
continues to feed : but, after a while, it abstains from
ingesting solid food and lives a simple, easy life, fed by
the products of the photosynthetic activity of its green
cells. Later on, unsatisfied with the amount or kind
of tribute which it thus receives, the animal begins to
digest its algal cells and may continue the habit until
the green tissue has, in larger measure, disappeared.
In the meantime, however, C. roscoffensis has matured
and produced eggs, the substance of which has been
supplied by the green cells ; so, even though it now
dies as the consequence of its ill-considered greedi-
ness, the continuance of the species is assured.

9—2

132 PLANT-ANIMALS [OH.

C. paradoxa exhibits a like behaviour. Though it
never becomes a total abstainer from ingested, solid
food, there are times when it makes inroads on its
yellow-brown cells, and indeed, if supplies of solid
food are withheld from it, C. paradoxa exhibits no less
scruple than C. roscoflfensis in raiding its algal cells.

But if C. roscoffensis is maintained in filtered sea-
water, and hence prevented from becoming infected
by its green algal associate, the course of events is
very different. Even though diatoms and other micro-
organisms are added to the filtered sea-water, C. ros-
coffensis, after a few days of active feeding, ceases from
ingesting solid food-substances. For a while, the fat
and other reserve food-substances contained in its body
suffice for the needs of the animal, but, when these
reserves are exhausted, starvation begins. In spite
of any addition of food-material to the filtered sea-
water — food-material which its infected green fellows
are enjoying — uninfected C. roscoflensis abstains
obstinately from ingesting it. It is waiting for the
development of its green tissues which ought by this
time to have been laid down in the body. Thus it
waits, and starves, dwindles till it has become in-
visible to the eye, and, ultimately, after weeks of
waiting, dies. If, before this happens, the algal in-
fecting organism is added to the water, the animal
may — should exhaustion be not too pronounced —
ingest it. Having thus achieved infection, it is a

v] NATURE OF PLAXT-ANIMALS 133

changed being. Activity takes the place of lethargy
and growth, of degeneration. In a few days it be-
comes, instead of a microscopic, transparent object, a
visible, green organism.

The immediate problem is, how to explain this
arbitrary behaviour of the uninfected organism. That
it is at once a pathetic tribute to the dependence
of C. roscoffensis on the infecting organism and a
justification of the title of this book, is evident.
Without the green cells, life to it is not worth living,
and it dies though surrounded by a plentiful micro-
flora of which in happier, infected circumstances it
avails itself without stint.

Let us suppose that the tenor of normal develop-
ment of an organism is not smooth and even, but
abruptly intermittent ; that in the complex business
of growing up — a business which involves many
simultaneous processes and many processes which are
necessarily consecutive — the consummation of one
phase serves as the signal for the commencement of
the next. Then, if, for one cause or another, one
process does not complete itself, there will be no
signal for the beginning of the consequent process.
So, in respect of this series of processes, the organism
never grows up. It exhibits the phenomenon of
arrested development. The signal for full steam
ahead with the next growth-process may be produced
internally ; or it may be of external origin. The ivy,

134 PLANT-ANIMALS [CH.

which grows on the wall, awaits in vain for the signal
of high light intensity which is required to call forth
the development of its flowers. Many plants exhibit
transient or permanent youth-forms ; that is, they
pass through or remain in juvenile stages of de-
velopment. A like phenomenon, with respect to the
organism as a whole, or with respect to single
organs is exhibited by animals and by man himself.
In the great number of cases, it is to be supposed
that the signal which is given or not given is of
internal origin. It is very probable that such signals
for development are of a chemical nature. The
important work of Starling (1906) has supplied
physiologists with a new method, capable of precise
application, in their work of analysing nervous
responses in animals and in plants. Thus, he has
demonstrated that a secretion may be the result, not
of a nervous stimulus, but of the arrival at the
secreting organ of a definite chemical substance.
To give but one illustration of Starling's discoveries :
some time after food has been swallowed, the pancreas
begins to discharge pancreatic juice into the small
intestine. Hence, the food, partially digested by the
stomach, is met, soon after its arrival in the small
intestines, by the pancreatic juice and acted on
in such a way that the materials it contains are
rendered soluble and diffusible and so capable
of passing into the blood-stream. This purposeful,

v] NATURE OF PLANT-ANIMALS 135

automatic process of the production of pancreatic
juice is independent of the nervous system. It occurs
in the absence of all nervous connections between
the intestines and pancreas. Now Starling has
shown that the stimulus which induces secretion in
the pancreas is due to a definite, chemical sub-
stance (secretin). This substance is produced in the
small intestine as the result of the passage of food
into that organ. It passes from the intestine into
the blood-stream, is carried to the pancreas and gives
the signal to that organ to commence its secretive
activity. Such specialised, chemical stimulators
Starling calls "hormones," and it is not to be doubted
that they play an important part in inducing large
numbers of normal processes which, as we know,
arise as the consequences of antecedent processes.
In plants in particular, it would seem that we must
look to hormones, or chemical stimulators to pro-
vide us with an understanding of many phenomena
which are at present ignored, or ascribed vaguely to
nervous action. For example, the living tissue in the
stem of plants, known as cambium, which is re-
sponsible, by continued growth and division, for the
increase in thickness of the stem, occurs in young
plants as definite, localised patches or sheets lying
between the vascular-bundles. After the plant has
reached a certain stage, the non-dividing cells of the
cortex which are coterminous with the cambium

136 PLANT-ANIMALS [CH.

cells, become, as it were, infected, and commence to
divide. Then cells neighbouring these begin to divide
and play the part of cambium, till finally a complete
ring or hollow cylinder of actively dividing cells is
formed in the stem ; and from this ring, which lasts
as long as the plant lives, are produced new wood
and new bast. Though no definite, chemical stimu-
lator has been discovered in this case, we may feel
sure that that is due to the fact that it has not been
sought.

Applying the conception of chemical stimulators
or hormones to the case of arrested development
exhibited by C. roscoffensis, we may suppose that in
this animal, the signal for the commencement of the
later phases of development owes its origin to the
presence, within the body of the animal, of the green
algal cells, that, in the absence of these cells, the
signal is not given, and that, consequently, develop-
ment does not proceed.

Hence it would follow that no amount of feeding,
either with diatoms or any other elements of the natural
micro-flora and fauna existing in the environment of
C. roscoffensis, can compensate for the lack of the
hormone entrusted by custom with the task of sig-
nalling to the animal to proceed with the business of
ordered development. On this view, the failure —
which has been complete — to rear C. roscoffensis on
artificial food, starch, sugar, peptone, protein, milk

v] NATURE OF PLANT- ANIMALS 137

and prepared "human foods" of various kinds, is
intelligible ; nor may we expect success to attend our
attempts to raise a colourless race of C. roscoifensis
till we have discovered the signalling substance pro-
duced by the green cells.

We turn now to another phenomenon exhibited by
larval C. roscoffensis. Considered attentively, the
rapid development of the green tissue in the infected
animal is no less remarkable than the arrest of develop-
ment in the uninfected animal. How comes it that
an alien organism, intruding itself among the tissues
of a young animal, is able to multiply so rapidly and
extensively therein? It might be supposed that it
was but a case of simple parasitism ; that the green
cell lives and multiplies directly at the expense of
the animal's cells. This, however, can scarcely be the
case, for, in their early stages at least, the green
cells keep themselves to themselves. They lie in
vacuolar spaces out of direct contact with the animal
cells. Hence any food-materials which they obtain
from the body of the animal must be in a state of
solution. Again, there is no evidence whatever that
the green cells obtain access to any soluble food-
substances which the animal has prepared for its
own use. The time during which the increase of the
green cells is greatest — soon after infection has taken
place — is also the time when the animal itself is
growing most rapidly. It is true that during this

138 PLANT-ANIMALS [CH.

period, the animal is ingesting solid food and there-
fore it is not impossible that the food-materials
obtained from this source may be shared alike by
the cells of the animal and the green, algal cells.
But, before we accept this view, we must enquire
into the conditions which obtain in the body of C.
roscoffensis at the time of infection, with the object
of ascertaining what sort of a "seed bed" for the
growth of the algal cells is provided by the body of
the animal.

The first fact which is brought to light by an
enquiry of this nature is that the association between
green cells and animal does not begin with the en-
trance of the green cell or its colourless antecedent
into the body. Before the relationship reaches this
condition of intimacy, animal and free green alga have
struck up an acquaintance based on the identity of their
mode of phototropistic response. Under the stimulus
of unilateral light, they both move in the direction
of the light and both proceed to the upmost edge of
the sea-water pools or streams in which they occur.
But this is not all. The free-living alga settles
down from time to time in the mucilage which forms
a slimy coating over the body of C. roscofFensis and,
withdrawing its flagella, passes into the condition of
a resting cell (Fig. 22). Inasmuch as the skin of the
animal provides the capsules which enclose the
clutches of eggs, it follows that, not infrequently, one

v] NATURE OF PLANT-ANIMALS 139

or more of the resting cells of the infecting organism
come to be included in the capsule- wall. Further,
apart from such chance inclusions, thanks to which
we were enabled to produce our pure cultures of the
alga, the egg-capsules appear to exert a definite
chemical attraction on the motile green cells. Thus,
if to a bulk of filtered sea-water containing egg-
capsules which have been laid under the cleanest
possible conditions, a number of the flagellated cells
are transferred, then, after a few hours, one or more
of the green cells will be found to have settled down
on each capsule. Yet more striking results are
obtained if a capsule is suspended in a hanging drop
—that is, a drop of sea-water which depends from
the under side of a microscope cover-glass — and if
a number of the flagellated cells are added to the
drop. On observing such a preparation under the
microscope, the motile green cells are seen to approach
the capsule, to swarm about it, to press in close ranks
into the soft, gelatinous wall and so embed themselves
in the envelope. We conclude, therefore, that the
egg-capsule exercises an attractive (chemotactic)
influence on the flagellated algal cells ; or, in other
words, that a definite substance diffusing out from
the capsule-walls induces a tropistic (tactic) move-
ment in the motile, algal cells of such a nature that
they approach the source whence the chemical sub-
stance emanates. The behaviour of the green cells,

140 PLANT-ANIMALS [CH.

which thus settle on and in the capsule, proves that
they find in it a favourable medium for growth.
Within a few hours, each green cell, having with-
drawn its flagella, increases considerably in size and,
whilst retaining its green colour, takes on a granular
appearance. The eye-spot and pyrenoid become
fainter and the cell undergoes division. In the
daughter cells thus produced, a series of successive
divisions occur till a loose colony of green cells is
formed — such a colony, in short, as that which enabled
us to determine the nature of the infecting organism
(p. 120). In egg-capsules, some of the eggs of which
have died, the green cells find yet richer supplies of
food-material and increase the more rapidly. These
observations give us a hint as to the nature of the
food-materials contained in the capsules, which serve
for the rapid increase in the green cells. For though,
as we have learned, green plants have at their com-
mand unlimited supplies of the raw materials, carbon-
dioxide and water, for the manufacture of carbo-
hydrates, they are by no means in so happy a situation
with respect to the raw materials for the synthesis of
organic, nitrogen-containing compounds. A green
plant growing with its roots in the soil, and relying
on inorganic salts — nitrate of potash, etc.— for its
supplies of nitrogen-containing, raw material, is often
hard put to it to obtain enough of these nitrogen
compounds wherefrom to manufacture its proteins,

v] NATURE OF PLANT-ANIMALS 141

and thus to augment its living substance, integral
parts of which consist of organic, nitrogen-containing
compounds. That such plants suffer not infrequently
from nitrogen-hunger is one of the most important
agricultural discoveries of the last century. As a
consequence of the recognition of this fact, many
thousands of tons of nitrate of soda from the nitrate
beds of S. America and equally vast quantities of
sulphate of ammonia — a bye-product of the distil-
lation of coal — are added annually by the farmer to
his land. Nor is the origin of this nitrogen-deficit
far to seek. The nitrogen contained in the nitrates
of the soil comes in the plant to form a constituent
of the organic nitrogen compounds, such as the pro-
teins. The plant dies and decays, or is eaten and
the eater decays. Ultimately, as the result of these
processes of decay, water and carbon-dioxide are
liberated and may at once be brought again, by the
agency of the green plant, into the vital circulation.
Synthesised to form carbohydrates, these substances
are once more available for the nutrition of plants
and animals. But with respect to nitrogen it is
otherwise. The organic nitrogen compounds of the
dead animal or plant are broken down by the bacterial
and fungous agents of decay into a series of simpler
forms which, acted on by yet other of the ordered
army of saprophytic micro-organisms, yield finally
ammonia and nitrogen. The nitrogen leaks away
into the atmosphere and contributes to the 79 per

142 PLANT-ANIMALS [CH.

cent, of nitrogen gas which is contained in the
air. The ammonia may leak away also — as every
dung-hill testifies — or it may be fixed in the soil
by the agency of certain nitrifying micro-organisms.
These bacteria convert the ammonia into nitrates
and the nitrates so formed become available to the
roots of the green plant. On the other hand, the
nitrates of the soil may be seized upon by yet other,
denitrifying micro-organisms and, becoming con-
verted into ammonia compounds, may be lost to the
vital circulation. The constant leakage of nitrogen
from combined forms to the free and inert form of
nitrogen gas results in a shortage of nitrogen available
for the formation of the nitrogenous food of plants.
We may thus speak of the problem which besets all
living organisms — that of obtaining adequate supplies
of organic nitrogen compounds — as the nitrogen
problem, and we may well believe that the sum-total
of life supported on our planet is determined ulti-
mately by the amount of available nitrogen present
in the earth and sea. Occasionally, organisms are
met with which have solved the nitrogen problem
in a fundamentally satisfactory manner. Among
such organisms are nitrogen-fixing bacteria, legu-
minous plants and man. Each of these organisms
has evolved methods of bringing back into vital
circulation the nitrogen which has escaped as nitrogen
gas into the air.

The nitrogen-fixing bacteria which occur in the

v] NATURE OF PLANT-ANIMALS 143

soil and also in the sea, possess the power of
causing free nitrogen to enter into combination with
other elements and so to serve as material for the
construction of the vitally necessary proteins. The
leguminous plants, clovers, peas, lupins, etc., do it —
or rather get it done for them — by entering into
association with a certain species of nitrogen-
fixing micro-organism. This organism, Pseudomonas
radicicola, enters the root and increases in its
tissues. Under the stimulus of this micro-organism,
the root swells locally to form nodules or tubercles.
Later, when the nodule-organism has accumulated
considerable quantities of organic, nitrogen com-
pounds, the tissues of the root destroy it, raid its
stores arid, living on the nitrogen-plunder, are able,
unlike other plants, to grow in soils which are
deficient or even lacking in inorganic, nitrogen com-
pounds. Thus, the gorse occupies vast tracts of
sterile, sandy wastes in Brittany and elsewhere, and
the traveller in spring may journey for miles between
tree-like groves of gorse ablaze with golden blossom,
every particle of which owes its presence in the air
to the nitrogen-fixing bacteria at work in the roots
underground. These bacteria it is which have provided
the essential, organic nitrogen compounds without
which the tissues of the flowers could not have been
formed. Large tracts of waste land in Germany,
America and other parts of the world have been

144 PLANT-ANIMALS [CH.

rendered amenable to cultivation by planting with
lupins. The roots of these plants, beset with nodules,
decay in the ground, release nitrogen-compounds,
hitherto deficient in the soil, and thus, by their decay,
admit of the growth of plants which rely entirely on
"fixed" or combined nitrogen. It is computed by com-
petent authorities that in Germany alone no less than
500 million pounds of nitrogen are secured annually
from the air through the activity of the root-tubercle
bacteria associated with leguminous crops.

It is a grim commentary on the mode and rate of
progress of agricultural science that these discoveries
of the men of science yesterday were among the
accepted commonplaces of the ancients. Thus Pliny
observes that "the bean ranks first among the legumes
and it fertilizes the ground in which it has been sown
as well as any manure."

Man solves the nitrogen problem by including
legumes in his crop-rotations, by transporting nitrates
from Chili to his European fields and — more re-
cently— by effecting a combination of the nitrogen
of the air with oxygen or other elements, utilising
for this purpose electrical energy. Where water-
power is available for the generation of electricity,
factories, destined to play an increasingly important
part in the solution of the nitrogen problem, are at
present at work turning out large quantities of cal-
cium nitrate or other nitrogen-containing compounds.

v] NATURE OF PLANT-ANIMALS 145

These compounds, put into the soil, are each a source
whence the green plant may obtain the raw materials
for the synthesis of organic nitrogen and thus increase
the supplies of material essential for the development
of brain and muscle in animals and man.

The fact of nitrogen-hunger is, then, no small matter
of mere academic importance. It touches the future
of man himself and presents a problem which every
living organism must solve. The supply of available
nitrogen is a limiting factor of life. Let us see what
bearings the fact of nitrogen-hunger have on the
economy of C. roscoffensis and C. paradoxa.

That nitrogen-hunger presses as hardly on marine
organisms as on those which live on the land is
undoubted. Recent investigations have shown that
the amount of combined nitrogen present in sea-
water, in a form available to plants for synthetic
purposes, is extremely low. Thus, according to
Johnstone (1907), the amount of nitrogen compounds
in Baltic and North Sea water may be taken as about
"2 millegrams (= '003 grains) in a litre, or about two
parts in a million. No wonder that marine animals
are always hungry ! No wonder either that the
free, flagellated infecting organism of C. roscoflensis
settles down on the egg-capsules to avail itself of any
crumbs of nitrogen compounds that it may find there.
Nor is it remarkable that, finding a certain amount

K. 10

146 PLANT-ANIMALS [CH.

of combined nitrogen, it begins to divide and soon
forms a colony of numerous green cells.

Now, as we have indicated previously, C. ros-
coffensis and C. paradoxa are remarkable among the
Turbellarian worms in possessing no excretory sys-
tem. Unlike their allies, they possess no apparatus
for the systematic discharge of the waste products of
their metabolism. Hence such products, compounds
of nitrogen of a kind useless to the animal, are stored
in the tissues of the body. But such substances,
though useless for the nutrition of the animal, serve
well for plants. Even a terrestrial green plant is
very catholic with respect to the compounds of nitro-
gen which it takes up and utilises for the synthesis
of proteins. Thus, experiment has shown that the
root-system of a green flowering plant is capable
of absorbing, not only nitrates and, in many cases,
ammonium salts, but also such organic, nitrogen-
containing substances as urea, uric acid, asparagine
and many others. Now the infecting organism of C.
roscoffensis occurs, as we know, in a colourless as well
as in a green stage, and, in the colourless form, it can
obtain its food materials only after the manner of an
animal, that is, in combined organic form. So that
its powers of taking up and utilising organic nitrogen
compounds are likely to be even more marked than
those of a self-supporting green plant. This con-

v] NATURE OF PLANT-ANIMALS 147

jecture is confirmed by experiment. Comparative

cultures of the free stage of the infecting organism

have demonstrated that the alga flourishes better when

supplied with nitrogen in the form of uric acid than

when it is supplied with a nitrate (potassium nitrate).

Thus our argument brings us to the following

position : We have evidence that the infecting

organism increases rapidly as soon as it gains access

to the body of the plant-animal. We know that it

is able to utilise organic nitrogen compounds such

as uric acid for the construction of its proteins. We

know, further, that no apparatus for the removal of

waste nitrogen compounds, uric acid, urea, etc., occurs

in the bodies of C. roscoffensis or C. paradoxa. The

conclusion forces itself upon us that the green and

yellow-brown cells in the bodies of their respective

hosts obtain access to and utilise the stores of waste

nitrogen-compounds accumulated therein. Or, to

put the same idea in another way, green cells and

yellow-brown cells constitute the excretory organs

of C. roscoffensis and of C. paradoxa respectively.

The plants flourish in the bodies of these animals

because there they discover large accumulations of

waste nitrogen compounds: the animals, looking to

the algse to come and take charge of the work of

getting rid of these waste substances, have ceased

to construct any excretory apparatus whatever.

Hence it is not surprising that, when the algse fail

10—2

148 PLANT-ANIMALS [OH.

to appear in their bodies, the animals suffer. It may
be that the death of uninfected animals is not merely
the consequence of starvation, but is at all events
hastened by poisoning due to the accumulation in
the tissues of the products of nitrogenous metabolism.
According to this view, uninfected C. roscoifensis dies
as the consequence of an aggravated attack of " uric
acid trouble."

Evidence is not lacking in support of this some-
what fantastic suggestion. Thus, if larval C. ros-
coffensis are protected from infection and kept without
food, as their large store of reserve food-material
derived from that contained in the eggs, disappears,
numerous vacuoles charged with long, acicular,
crystalline bodies make their appearance in the
tissues. The vacuoles and crystals increase in
numbers till they present a most striking appear-
ance. These crystals represent, in all probability,
the waste products of nitrogen-metabolism.

Now, in infected animals, the crystalline bodies
do not occur, and if animals in which they are present
are caused to become infected by the green algal
cells, the crystals disappear as fast as the green cells
develop. Whence we may infer that the materials
of which the crystalline bodies consist are used for
the nutrition of the green cells.

The evidence which C. roscoffensis provides in
favour of our hypothesis is, of course, but slender.

v] NATURE OF PLANT-ANIMALS 149

Let us appeal therefore to C. paradoxa. A far more
greedy feeder than the green species, its accumula-
tions of nitrogenous waste substances are much larger
than are those of its ally. Inspection of the Frontispiece
or of Fig. 4 shows well-marked, granular bands across
the body of the animal. These bands consist prob-
ably, as von Graff has suggested, of urates. They
are slight in the young animal, increase as it matures,
but may disappear as the period of egg-laying arrives,
at which time the yellow-brown cells have developed
to their full extent.

In order to establish our hypothesis we must
demonstrate that the yellow-brown cells of C. para-
doxa actually make use of such substances — pre-
sumably uric acid or urates — as are stored in the
body.

For this purpose, two modes of experimentation
were adopted. In the first method, batches of animals
of similar sizes and origin were maintained in the
light in filtered sea-water to which uric acid was
added and their condition was compared with that
of animals kept in filtered sea-water containing no
uric acid. Preliminary observations showed that the
uric acid added to the sea- water was taken up readily
by the animals and stored in vacuoles in the tissue
of the digestive tract. Examination and measurement
of animals from the two batches — those in filtered
sea-water only and in filtered sea-water plus uric

150 PLANT-ANIMALS [OH.

acid — proved that the latter were, after twenty-one
days, considerably larger than the former.

The experiment was continued. During the follow-
ing weeks the animals in filtered water, dwindled, lost
all their yellow-brown cells, became of microscopic
size and died. On the other hand, after upwards of
thirteen weeks, specimens of the animals in filtered
water plus uric acid were alive, of a recognisably
brown colour and possessed of many normal, yellow
brown cells.

We thus have proof that when C. paradoxa is
kept in the light, so that its yellow-brown cells may
photosynthesise, and when uric acid is supplied, this
substance serves as a source of nitrogen to the yellow-
brown cells. Moreover, in these circumstances, the
materials manufactured by the yellow-brown cells
serve not only for the nutrition of the alga but also
for that of the animal. This, however, means that
the yellow-brown cells contribute not only fatty but
also nitrogenous, protein-forming material to the
animal. That this is the case the results of the
second mode of experimentation render highly
probable.

Here, in lieu of determining the effect of uric
acid on the life of algal cell and animal, its influence
on egg-laying was investigated. The experiment
consisted in maintaining equal numbers of similar
animals in filtered sea- water, under conditions which

v] NATURE OF PLANT-ANIMALS 151

were identical except for the fact that one lot received
uric acid. The animals supplied with no extra nitrogen
laid nine clutches of eggs, whereas the animals sup-
plied with extra nitrogen laid twenty-seven clutches.
The results of the two sets of experiments just
described serve to account for the rich development
of algal cells within the bodies of the plant-animals.
In their free state, these algse, like all marine plants,
run grave and frequent risk of nitrogen-starvation,
or at all events of having their increase limited by
the shortage of available nitrogen in the sea. Wherever
there is any leakage of nitrogen compounds — and
traces of combined nitrogen must be given off from
such animals of C. roscoffensis and C. paradoxa —
marine, motile plants will congregate. Congregating
about our plant-animals, such minute organisms are
ingested indifferently. Out of this mixed infection C.
roscoffensis and C. paradoxa make each a pure culture,
the one of green cells the other of yellow-brown cells.
Established in the body, the algal cells find them-
selves transferred from a region of scarcity to a land
of plenty. Outside, in the open sea, the amount of
nitrogen available is but small and the claimants for
a share of it innumerable : within the body, the
amount of suitable, combined nitrogen is large and
at the exclusive disposal of the algal visitors. In
such Capuan circumstances, the algal cells grow and
divide luxuriantly. Their photosynthetic activities

152 PLANT-ANIMALS [OH.

increase, for only in the presence of plentiful sup-
plies of nitrogen does the chlorophyll-apparatus work
well. Large quantities of carbohydrate material
are produced in the algal cells — enough for the needs
of these cells and also for those of the animal. All
goes well, so well indeed that C. roscoffensis, less
conservative than its ally, contents itself entirely
with the supplies of food-material, of fat and also
of organic nitrogen compounds, provided by its green
cells and abandons the practice of fending for itself.
The ample tribute which it receives suffices for its
needs and also for the provision of its eggs. But the
weakness of the system here discloses itself. This
handing of nitrogen-containing substances to and fro
from animal to plant and from plant again to animal
cannot go on indefinitely or without loss. Sooner or
later, the animal finds itself lacking in essential,
nitrogen-containing food-materials. Supply fails to
equal the demand. Then the animal is under the dire
necessity of digesting its algal cells. To satisfy an
imperious, present need, the plant-animal destroys
the source of its supplies.

Thus the animal repudiates the association and,
having digested its green cells, C. roscoffensis dies
of the very complaint — nitrogen-hunger — which the
green cells sought to avoid by their intrusion into
the body of the animal. To dismiss the association
between animal- and plant-constituent of the plant-

v] NATURE OF PLANT-ANIMALS 153

animals by labelling it symbiosis is to miss the vary-
ing significance of the association. Looking at the
relationship from the standpoint of the animal, it is
one of obligate parasitism. Apart from their algal
cells, C. roscoffensis and C. paradoxa are unable to
live. The existence of either species depends upon
the infection of the individuals of each successive
generation. Where the infecting organism is absent,
there C. roscoffensis does not exist. Hence its re-
stricted range. From the standpoint of the species,
"infecting organism," the relation of certain of its
individuals with C. roscoffensis or C. paradoxa is an
episode without significance. Unlike the animal,
which bears the inherited impress of the relation
in lack of excretory system and in the habit of
patient waiting — abiding the question of infection —
the alga is free. Of a swarm of flagellated green
cells, some small percentage meet the picturesque
fate of forming a tissue in the body of an animal.
The others pursue a less romantic adventure, either
as green, self-supporting organisms or as colourless
cells which batten on the offal of the sea.

From the standpoint of the ingested algal cell,
association with the animal means a successful solu-
tion of the nitrogen problem. It sacrifices its
independence for a life of plenty. This universal
nitrogen-hunger is a misery which makes strange
bed-fellows.

10—5

154 PLANT-ANIMALS [OH.

It is noteworthy that the interpretation, in terms
of the hypothesis of nitrogen-hunger, of the relation
between animal and algal cell throws light on the
facts, already referred to, concerning the distribution
of algal cells in various marine animals. Analyses
have demonstrated (Johnstone, 1907) that the amount
of combined nitrogen present in sea-water is less
during the warm months (e.g. August) than during
the cold months of the year, and that it is less
in the warmer seas (Mediterranean) than in the
colder seas (Baltic and North Sea). Now, as we
have mentioned, certain animals possess green or
brown algal cells in one part of their range of dis-
tribution but lack them in other parts. Thus
Noctiluca, colourless in the North Atlantic, is green
in the Indian Ocean. Whence it would appear to
follow that where the stress of nitrogen-hunger is
more acute, there the association between algal cells
and animals manifests itself.

One word more and one more speculation and our
work is done. The colourless phase in the life-history
of the infecting organism of C. roscofiensis, the colour-
less state of the just-ingested algal cells both in
C. roscoifensis and C. paradoxa, and the rapid as-
sumption of their proper pigments by the infecting
cells after they are established in their respective
animal quarters suggest that the colourless phase is
itself the outcome of nitrogen hunger. Such colour-

v] NATURE OF PLANT-ANIMALS 155

less phases are known to occur in the life histories
of other micro-organisms, in diatoms, in various species
of Chlamydomonas and in Flagellates (Euglena), and
it is stated generally that they may be induced by
increasing the amount of soluble carbohydrate in
the culture medium. But in the cases of the algal-
infecting organisms of our plant-animals, the rapid
development of the chlorophyllous pigment appears
to be associated with the increase in the amount of
available nitrogen. So that, if this is the case, the
colourless phase would appear to be brought about,
not by excess of food-material, but by lack of nitrogen.
It may well prove to be that the colourless sapro-
phytic phases exhibited by such organisms as those
just mentioned — diatoms, etc. — are each a symptom
of nitrogen-hunger. For, failing proper supplies of
nitrogen compounds, no amount of carbohydrate photo-
synthesis will keep the organism from starvation.
Indeed, the more the carbohydrate photosynthesis, in-
volving as it must the wearing out and reconstruction
of the nitrogen-containing chlorophyll machinery, the
acuter will be the nitrogen-hunger ; whereas, on the
contrary, a shutting down of the photosynthetic process
will effect economies in the use of organic nitrogen
compounds and thus postpone the evil day of nitrogen-
starvation. Though the facts are not yet available
for a confident statement, the hypothesis may be
proposed that saprophytism generally depends for

156 PLANT-ANIMALS [OH.

its inception on nitrogen-hunger. It is tempting
to push this hypothesis to its limits, and to imagine
that the great saprophytic groups of the fungi
and the bacteria owe their origin to the changed
mode of nutrition imposed upon them by lack of
nitrogen. That the fungi are examples of descent
by reduction is undisputed. All the evidence points
to their derivation from chlorophyll-containing algal
ancestors. Having lost their chlorophyll, and, with
it, their powers of photosynthesis, they are now con-
demned to obtain both carbon and nitrogen in the
form of organic compounds and hence are compelled,
with the bacteria, to play the part of Nature's
scavengers. In their quest for food, they settle
either on the dead remains of plants or animals,
or, invading the living organism, they exchange a
saprophytic for a parasitic mode of life.

The hypothesis suggested here is that the first
and fatal step from independence to dependence was
the outcome of the nitrogen scarcity which exists
in Nature. Confronted with indequate supplies of
nitrogen, the photosynthetic activity of their chloro-
phyll apparatus was brought to a standstill. The
organisms, unable to obtain supplies of inorganic
nitrogen compounds, were constrained to resume their
powers, never wholly lost, of absorbing nitrogen com-
pounds in organic form. But such organic nitrogen-
containing compounds contain also carbon. Hence

v] NATURE OF PLANT-ANIMALS 157

supplies of this element were obtained together with
nitrogen. In these circumstances, the expensive chlo-
rophyll apparatus ceased to be worth its upkeep and,
wearing out, proved to be too costly in nitrogen to be
replaced. Thus the organism, now devoid of chloro-
phyll, was reduced to a condition in which it obtains
directly from its environment as much carbon in
combined form as is of use to it and as much combined
nitrogen as it can get. It has become a saprophyte.

Should this hypothesis of the origin of sapro-
phytism be established, C. roscoffensis and C. para-
doxa will rank high in interest among organisms as
suggesting the route along which far-reaching evo-
lution has travelled. In any case, it may be claimed
for our plant-animals that they have anticipated the
advice of Candide and live to cultivate their gardens.

Both C. roscoifensis and C. paradoxa possess self-
sown, well-tended, highly productive gardens, and if
they could but learn how to bequeath packets of
vegetable seed to their descendants, they might lose
their animal characteristics altogether and become,
C. roscoffensis a green plant, and C. paradoxa a yellow-
brown plant. As it is, the garden has to be replanted
in the individuals of the successive generations and
so they remain plant-animals.

BIBLIOGRAPHY

For more complete lists of the literature dealing with the
subject of symbiosis between animals and plants see the Biblio-
graphies attached to the memoirs published by Messrs Gamble
and Keeble in the Quarterly Journal of Microscopic Science
(1903, 1907, 1908).

1879. Geddes, P. Observations on the Physiology and Histology
of Convoluta Schultzii. Proc. Roy. Soc. xxvm. pp. 449 — 457.

1880. Darwin, C. and F. The Movements of Plants, p. 523.

1898. Williams, J. Lloyd. Reproduction in Dictyota dichotoma.
Ann. of Bot. xn. pp. 559—560, 1898; and The Periodicity of
the sexual cells in Dictyota dichotoma. Ann. of Bot. xix.
pp. 531—560. 1905.

1900. Goebel. Organography of Plants. Eng. Trans. Univ.
Press, Oxford, p. 244.

1903. Bohn, G. Sur les mouvements oscillatoires des Convoluta
roscoffensis. C. R. Ac. Sc. Oct. 1903.

1903. Gamble, F. W. and Keeble, F. The Binomics of Convoluta
roscoffensis. Q. J. M. S. LVII. 1903.

1904. Semon, R. Die Mneme. W. Engelmann. Leipzig, 1904.

1906. E. H. Starling. Recent Advances in the Physiology
of Digestion. London, 1906.

1907. Johnstone. The Law of the Minimum in the Sea. Sci.
Progress, n. No. 6. Oct. 1907 ; and Life in the Sea. Univ.
Press, Cambridge. Biological Series.

160 BIBLIOGRAPHY

1907. Keeble, F. and Gamble, F. W. The Origin and Nature of
the Green Cells of Convoluta roscoffensis. Q. J. M. S. LI.
Part 2. 1907-

1908. Keeble, F. The Yellow-brown cells of Convoluta paradoxa.
Q. J. M. S. LII. Part 4. 1908.

1909. Loeb, J. Experimental study of the influence of Environ-
ment on Animals. Essay in Darwin and Modern Science.
Univ. Press, Cambridge.

INDEX

Alcyonium (British), 101
Alcyonium ceylonicum, 101

Bohn, G., 64
Butler, Samuel, 49

Carteria sp., 129
Chemical stimulators (hormo-
nes), 135

Chernotactism, 139
Chlamydomonadineae, 128
Chlamydomonas, 129
Chlorophyll, 87
Chloroplast, 85, 86, 105
Convolute paradoxa :

Background, influence of, 45,
48, 50

Behaviour in constant dark-
ness, 65

Bristles, 8

Cilia, 7

Digestion of green cells by,
83, 97

Digestive system, 11

Eggs, 13; periodicity of pro-
duction of, 24

Egg-laying, conditioned by il-
lumination, 31

Eyes, 9, 54

Fat, 89

Feeding habits, 81, 83, 97, 98

Convolute paradoxa (cont.):
General aspect, 5
Glands (pigmented), 9, 54
Gravi-perception, 10
Gullet, 11
Habitat, 7, 19
Mouth, 11
Otocyst, 9
Paradoxa zone, 17
Periodicity of egg-laying, 24,

34

Phototropism, 42
Secretion of fat by yellow-
brown cells of, 92
Starvation, resistance to, 94
Tidal migration, 21
Tropistic response to light,

42
Uric acid, effects on egg-laying,

150

Vacuoles, 11
Yellow-brown cells of, 75, 84,

91, 95, 147
Convoluta roscoffensis :

Background, influence of, 45,

48, 50

Chlorophyll in, 87
Cilia, 7
Dark-rigor, 60
Digestion of yellow-brown cells

by, 95

162

INDEX

Convoluta roscoffensis (cont.) :
Digestive system, 11
Eggs and egg-capsules, 13, 56 ;

periodicity of laying of, 26
Excretory organs (absence of),

147

Eyes, 9

Feeding habits of, 77, 81, 97
General aspect, 5
Gravi-perception, 10, 39
Green cells of, 75, 84, 105;

algal nature of, 118; life

history of, 132; origin, 108
Gullet, 11
Habitat, 7, 14, 18
Light-rigor, 60
Mouth, 11
Nucleus, 110

Nuclear degeneration, 112
Otocyst, 9
Periodicity of ascent, 62; of

egg-laying, 26
Photosynthesis by the green

cells of, 81, 87
Phototonic effect of stimulation,

59

Phototonus, 59
Phototropism, 41, 52
Keaction to monochromatic

light, 54

Eegeneration of, 27
Kesponse to vibration, 15
Ehythmic ascent and descent,

19, 62

Koscoffensis zone, 17
Simultaneous stimuli, 44, 45
Size, 16

Starch in green cells, 87
Starvation, resistance to, 94
Tidal rhythm, 63, 67
Tonic influence of light, '67
Tropistic response to light, 41

Convoluta roscoffensis (cont.) :

Vacuoles, 11

Vibration, response to, 62,

67
Copepods, tropism of, 69

Dictyota dichotoma, 34
Directive stimuli, 40

Echinocardium sp., 100
Elysia sp., 100
Eudendrium racemosum, 33
Euglena viridis, 103
Eye-spot, 102, 110

Flagella, 124
Fungi, 156

Geddes, P., 87

Goebel, K., 33

Gravi-perception (by roots), 38

Green cells of animals, 82,
100

Green cells of C. roscoffensis,
algal nature of, 128; colourless
phase of, 126; cultivation of,
115 ; structure and life history,
110, 123

Green light, and marine organ-
isms, 54

Haberlandt, G., 105
Hering, Prof. E., 49
Hippolyte varians, 47
Hormones, 135
Hydra viridis, 100

Ivy, 32

Lankester, Sir Bay, 114
Leucoplast, 105, 109
Lichens, 107

INDEX

163

Light, influence of, on plants, 32 ;

on regeneration of polyps, 33
Loeb, J., 29, 69

Macrocytes, 124

Microcytes, 124

Mneme (memory hypothesis), 49

Monochromatic light, 54

Mysis sp., 47

Nervous impulses, 39
Nitrogen-compounds in sea-water,

145, 154

Nitrogen-fixing bacteria, 143
Nitrogen-hunger, 145
Nitrogen-problem, 142
Noctiluca, coloured cells of, 101

Otocyst, 9

Palmella, 128

Photosynthesis by green plants,

78; by C. roscoffensis, 87
Phototropism of Copepods, 69
Prawns, 45
Protoplast (cell), 79
Pseudomonas radicicola, 143
Pyrenoid, 85

Keflex action, 43

Keflex arcs, 40

Reproduction, periodicity of, in

brown sea-weeds, 34
Ehizobium leguminosarum ( =

Pseudomonas radicicola), 143
Roscoffensis zone, 17

Salamandra atra, 29

S. maculosa, 29

Saprophytism, origin of, 157

Schimper, A. F. W., 114

Secretion, 135

Semon, R., 48

Simultaneous stimulation, 54

Starch, 87

Starling, E. H., 134

Starvation, 94

Symbiosis, 106, 143, 153

Tactic response to stimulation,

41
Tonic effect of light-stimulation,

58, 67
Tropistic response to stimulation,

41, 69

Unconscious memory, 49
Uric acid, absorption of, by C.
paradoxa, 149

Vacuoles (digestive), 11
Von Graff, 149
Vochting, H., 33

Williams, J. L., 34

Yellow-brown cells of animals,
82, 100 ; of C. paradoxa, 75, 84,
91, 95, 147

Zoobothrium sp., 100
Zoochlorella, 101, 105
Zooxanthella, 101

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